Abstract
We examined the effects of mechanical load on transcripts of a set of cell wall related genes that are implicated in the formation of supporting tissues, by applying a 50 mg strip of aluminum foil to the inflorescence stem of Arabidopsis thaliana, a weight roughly half the fresh weight of the stem. Transcript levels of 12 of the 15 genes examined were increased by load application, as were the levels of some transcription factors that regulate secondary wall formation. These findings support the involvement of a load-sensing system in regulation of supporting tissue formation via transcriptional regulation of cell wall related genes.
Abbreviations
- GUS:
-
β -Glucuronidase
- RT-PCR:
-
Reverse-transcription polymerase chain reaction
References
Batiza AF, Schulz T, Masson PH (1996) Yeast respond to hypotonic shock with a calcium pulse. J Biol Chem 271:23357–23362
Blee KA, Choi JW, O’Connell AP, Schuch W, Lewis NG, Bolwell GP (2003) A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry 64:163–176
Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389
Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364
Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295
Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y (2006) Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot 57:2563–2569
Chan C-S, Guo L, Shih M-C (2001) Promoter analysis of the nuclear gene encoding the chloroplast glyceraldehyde-3-phosphate dehydrogenase B subunit of Arabidopsis thaliana. Plant Mol Biol 46:131–141
Chehab EW, Eich E, Braam J (2009) Thigmomorphogenesis: a complex plant response to mechano-stimulation. J Exp Bot 60:43–56
Clough SJ, Bent AF (1998) Floral dip, a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Fukaki H, Fujisawa H, Tasaka M (1996) Gravitropic response of inflorescence stems in Arabidopsis thaliana. Plant Physiol 110:933–943
Giuliano G, Pichersky E, Malik VS, Timko MP, Scolnik PA, Cashmore AR (1988) An evolutionarily conserved protein binding sequence upstream of a plant light-regulated gene. Proc Natl Acad Sci USA 85:7089–7093
Hoson T, Soga K (2003) New aspects of gravity responses in plant cells. Int Rev Cytol 229:209–244
Hoson T, Nishitani K, Miyamoto K, Ueda J, Kamisaka S, Yamamoto R, Masuda Y (1996) Effects of hypergravity on growth and cell wall properties of cress hypocotyls. J Exp Bot 47:513–517
Iida H, Nakamura H, Ono T, Okumura MS, Anraku Y (1994) MID1, a novel Saccharomyces cerevisiae gene encoding a plasma membrane protein, is required for Ca2+ influx and mating. Mol Cell Biol 14:8259–8271
Iliev EA, Xu W, Polisensky DH, Oh MH, Torisky RS, Clouse SD, Braam J (2002) Transcriptional and posttranscriptional regulation of Arabidopsis TCH4 expression by diverse stimuli. Roles of cis regions and brassinosteroids. Plant Physiol 130:770–783
Imoto K, Yokoyama R, Nishitani K (2005) Comprehensive approach to genes involved in cell wall modifications in Arabidopsis thaliana. Plant Mol Biol 58:177–192
Jaffe MJ (1973) Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. Planta 114:143–157
Jaffe MJ, Forbes S (1993) Thigmomorphogenesis: the effect of mechanical perturbation on plants. Plant Growth Regul 12:313–324
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions, β-glucuronidase as a sensitive and versatile gene fusion maker in higher plants. EMBO J 6:3901–3907
Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478
Kanzaki M, Nagasawa M, Kojima I, Sato C, Naruse K, Sokabe M, Iida H (1999) Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285:882–886
Ko J-H, Han K-H, Park S, Yang J (2004) Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135:1069–1083
Ko J-H, Yang SH, Park AH, Lerouxel O, Han K-H (2007) ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana. Plant J 50:1035–1048
Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860
Le Gourrierec J, Li YF, Zhou DX (1999) Transcriptional activation by Arabidopsis GT-1 may be through interaction with TFIIA–TBP–TATA complex. Plant J 18:663–668
Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW (2000) A homolog of voltage-gated Ca2+ channels stimulated by depletion of secretory Ca2+ in yeast. Mol Cell Biol 20:6686–6694
Martzivanou M, Hampp R (2003) Hyper-gravity effects on the Arabidopsis transcriptome. Physiol Plant 118:221–231
Matsui A, Yokoyama R, Seki M, Ito T, Shinozaki K, Takahashi T, Komeda Y, Nishitani K (2005) AtXTH27 plays an essential role in cell wall modification during the development of tracheary elements. Plant J 42:525–534
Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Nakagawa Y, Katagiri T, Shinozaki K, Qi Z, Tatsumi H, Furuichi T, Kishigami A, Sokabe M, Kojima I, Sato S, Kato T, Tabata S, Iida K, Terashima A, Nakano M, Ikeda M, Yamanaka T, Iida H (2007) Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc Natl Acad Sci USA 104:3639–3644
Nishitani K, Hoson T, Kamisaka S, Yamamoto R, Masuda Y, Yamashita M (1992) Effect of gravity on plant growth and cell wall properties. Proc Int Symp Space Technol Sci 8:2109–2114
Palaniswamy SK, James S, Sun H, Lamb RS, Davuluri RV, Grotewold E (2006) AGRIS and AtRegNet. A platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiol 140:818–829
Soga K, Wakabayashi K, Kamisaka S, Hoson T (2004) Graviperception in growth inhibition of plant shoots under hypergravity conditions produced by centrifugation is independent of that in gravitropism and may involve mechanoreceptors. Planta 218:1054–1061
Szyjanowicz PMJ, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740
Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–780
Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100:1450–1455
Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50:43–56
Tsukaya H, Ohshima T, Naito S, Chino M, Komeda Y (1991) Sugar-dependent expression of the CHS-A gene for chalcone synthase from Petunia in transgenic Arabidopsis. Plant Physiol 97:1414–1421
Waldron KW, Brett CT (1990) Effects of extreme acceleration on the germination, growth and cell wall composition of pea epicotyls. J Exp Bot 41:71–77
Wenzel CL, Hester Q, Mattsson J (2008) Identification of genes expressed in vascular tissues using NPA-induced vascular overgrowth in Arabidopsis. Plant Cell Physiol 49:457–468
Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664
Yokoyama R, Nishitani K (2001) A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant Cell Physiol 42:1025–1033
Yokoyama R, Nishitani K (2006) Identification and characterization of Arabidopsis thaliana genes involved in xylem secondary cell walls. J Plant Res 119:189–194
Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1540
Zeidler D, Zähringer UZ, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana: Lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. Proc Natl Acad Sci USA 101:15811–15816
Zhao C, Avci U, Grant EH, Haigler CH, Beers EP (2008) XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53:425–436
Zhong R, Kays SJ, Schroederb BP, Ye Z-H (2002) Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 14:165–179
Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170
Zhong R, Richardson EA, Ye Z-H (2007) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611
Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–2782
Acknowledgments
We thank Ms. Kei Saito for her technical assistance in generating transgenic Arabidopsis lines. This work was supported by a grant-in-aid for Scientific Research on Priority Areas (19039003) to K.N. and by a grant-in-aid for Scientific Research (B) (19370014) to K.N. and (C) (19570030) to R.Y. from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10265_2009_251_MOESM1_ESM.tif
Fig. S1. Promoter::GUS expression profiles of each of the 15 genes in Arabidopsis. The genes were categorized as in Fig. 1. The left side of each panel shows flowers of inflorescence stems that reached a length of 100 mm, while the right side shows the third or fourth leaf of a 2-week-old plant. Most genes were expressed in anthers and leaf vessels. Bar 1 mm (TIFF 6035 kb)
10265_2009_251_MOESM2_ESM.tif
Fig. S2. Effects of load application on promoter::GUS expression patterns for CesA7 (a, b) and CesA4 (c, d) genes. A 15 mg (a, c) or 50 mg (b, d) of half-folded aluminum foil weight was attached to the inflorescence stem as shown in Fig. 1d. After the plants were allowed to grow for 2 days, region I (Fig. 1d) of the inflorescence was cross-sectioned and subjected to GUS staining. No apparent change in the expression pattern of the two genes was observed. Bar 200 μm (TIFF 2720 kb)
10265_2009_251_MOESM3_ESM.tif
Fig. S3. Promoter::GUS expression patterns of CesA7 (a–d) and CesA4 (e–h) along the inflorescence stem, 50 mm (a, e), 100 mm (b, f), 150 mm (c, g) and 200 mm (d, h) below the apex. Note that each of the two genes exhibits similar tissue specific expression pattern among the four regions along developmental stages of the inflorescence stem. Bar 200 μm (TIFF 5045 kb)
10265_2009_251_MOESM4_ESM.tif
Fig. S4. Effects of load application on histological pattern of the inflorescence stem. A 50 mg (a) or 15 mg (b) of half-folded aluminum foil weight was attached as shown in Fig. 1d. After the plants were allowed to grow for 5 days, region I (Fig. 1d) of the inflorescence stem was cross-sectioned and subjected to staining with 2% phloroglucinol-HCl to visualize tissues with secondary wall deposition. Bar 200 μm (TIFF 1775 kb)
Rights and permissions
About this article
Cite this article
Koizumi, K., Yokoyama, R. & Nishitani, K. Mechanical load induces upregulation of transcripts for a set of genes implicated in secondary wall formation in the supporting tissue of Arabidopsis thaliana . J Plant Res 122, 651–659 (2009). https://doi.org/10.1007/s10265-009-0251-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-009-0251-7