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A principal role for AtXTH18 in Arabidopsis thaliana root growth: a functional analysis using RNAi plants

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Abstract

Rearrangement of cellulose microfibrils within cell-wall matrices is considered one of the most critical steps in the regulation of both the orientation and extent of cell expansion in plants. Xyloglucan endotransglucosylase/hydrolases (XTHs) are a family of enzymes that mediate the construction and restructuring of load-bearing cross links among cellulose microfibrils. The Arabidopsis thaliana XTH genes AtXTH17, 18, 19, and 20 are phylogenetically closely related to one another and are preferentially expressed in the roots. However, they exhibit different expression profiles within the root and respond to hormonal signals differently. To investigate their functions in root growth, we examined phenotypes of loss-of-function mutants for these genes using T-DNA insertion lines and RNAi plants. These functional analyses disclosed a principal role for the AtXTH18 gene in primary root elongation. Of the four XTH genes, AtXTH18 exhibits the highest level of mRNA expression. We also determined auxin-signaling pathways for these genes using a mutant with a defect in the AXR2/IAA7 gene and found that the expression of AtXTH19 in the elongation/maturation region of the root is under the control of the AXR2/IAA7 signaling pathway.

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References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  PubMed  Google Scholar 

  • Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. J Biol Chem 270:19093–19099. DOI 10.1074/JBC.270.32.19093

    Article  PubMed  Google Scholar 

  • Akamatsu T, Hanzawa Y, Ohtake Y, Takahashi T, Nishitani K, Komeda Y (1999) Expression of endoxyloglucan transferase genes in acaulis mutants of Arabidopsis. Plant Physiol 121:715–722

    Article  PubMed  Google Scholar 

  • Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152. DOI 10.1126/science.284.5423.2148

    Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. DOI 10.1016/0003-2697(76)90527-3

    PubMed  Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30. DOI 10.1046/j.1365-313X.1993.00999.x

    Article  PubMed  Google Scholar 

  • Catala C, Rose JKC, York WS, Albersheim P, Darvill AG, Bennett AB (2001) Characterization of a tomato xyloglucan endotransglycosylase gene that is downregulated by auxin in etiolated hypocotyls. Plant Physiol 127:1180–1192

    Article  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. DOI 10.1046/j.1365-313x.1998.00343.x

    Article  PubMed  Google Scholar 

  • Cosgrove DJ (1997a) Assembly and enlargement of the primary cell wall in plants. Ann Rev Cell Devel Biol 13:171–201

    Article  Google Scholar 

  • Cosgrove DJ (1997b) Relaxation in a high-stress environment—the molecular basis of extensible cell walls and cell enlargement. Plant Cell 9:1031–1041

    Article  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445. DOI 10.1038/nature03543

    Article  PubMed  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation (2004). Trend Plant Sci 9:302–308

    Article  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451. DOI 10.1038/nature03542

    Article  PubMed  Google Scholar 

  • Fry SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol 161:641–675. DOI 10.1111/j.1469-8137.2004.00980.x

    Article  Google Scholar 

  • Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    PubMed  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  PubMed  Google Scholar 

  • Gil P, Liu Y, Orbovic V, Verkamp E, Poff KL, Green PJ (1994) Characterization of the auxin-inducible SAUR-AC1 gene for use as a molecular genetic tool in Arabidopsis. Plant Physiol 104:777–784

    Article  PubMed  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573. DOI 10.1104/pp.103.034736

    Article  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276. DOI 10.1038/35104500

    Article  PubMed  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Google Scholar 

  • Hyodo H, Yamakawa S, Takeda Y, Tsuduki M, Yokota A, Nishitani K, Kohchi T (2003) Active gene expression of a xyloglucan endotransglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol Biol 52:473–482. DOI 10.1023/A:1023904217641

    Google Scholar 

  • Iliev EA, Xu W, Polisensky DH, Oh M-H, 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. DOI 10.1104/pp.008680

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ito H, Nishitani K (1999) Visualization of EXGT-mediated molecular grafting activity by means of a fluorescent-labeled xyloglucan oligomer. Plant Physiol 40:1172–1176

    Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  Google Scholar 

  • 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. DOI 10.1111/j.1365-313X.2005.02395.x

    Article  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–496

    Google Scholar 

  • Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encode a member of the Aux/IAA protein family. Plant Physiol 123:563–573

    Article  PubMed  Google Scholar 

  • Nakamura T, Yokoyama R, Tomita E, Nishitani K (2003) Two azuki bean XTH genes, VaXTH1 and VaXTH2, with similar tissue-specific expression profiles, are differently regulated by auxin. Plant Cell Physiol 44:16–24

    Article  PubMed  Google Scholar 

  • Nishitani K (1997) The role of endoxyloglucan transferase in the organization of plant cell walls. Int Rev Cytol 173:157–206

    PubMed  Google Scholar 

  • Nishitani K (2002) A genome-based approach to study the mechanisms by which cell-wall type is defined and constructed by the collaborative actions of cell-wall-related enzymes. J Plant Res 115:303–307. DOI 10.1007/s10265-002-00032-z

    Article  PubMed  Google Scholar 

  • Nishitani K, Masuda Y (1981) Auxin-induced changes in the cell wall structure: changes in the sugar compositions, intrinsic viscosity and molecular weight distribution of matrix polysaccharides of the epicotyl cell wall of Vigna angularis. Physiol Plant 52:482–494

    Google Scholar 

  • Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267:21058–21064

    PubMed  Google Scholar 

  • Okazawa K, Sato Y, Nakagawa T, Asada K, Kato I, Tomita E, Nishitani K (1993) Molecular cloning and cDNA sequencing of endoxyloglucan transferase, a novel class of glycosyltransferase that mediates molecular grafting between matrix polysaccharides in plant cell walls. J Biol Chem 268:25364–25368

    PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis T (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463

    Google Scholar 

  • Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995) Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139:1393–1409

    PubMed  Google Scholar 

  • Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868

    Article  PubMed  Google Scholar 

  • Vissenberg K, Martinez-Vilchez IM, Verbelen J-P, Miller JG, Fry SC (2000) In vivo co-localization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of Arabidopsis roots. Plant Cell 12:1229–1237

    Google Scholar 

  • Vissenberg K, Fry SC, Verbelen JP (2001) Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiol 127:1125–1135

    Article  PubMed  Google Scholar 

  • Vissenberg K, Van Sandt V, Fry SC, Verbelen J-P (2003) Xyloglucan endotransglucosylase action is high in the root elongation zone and in the trichoblasts of all vascular plants from Selaginella to Zea mays. J Exp Bot 54:334–344. DOI 10.1093/jxb/erg024

    Article  Google Scholar 

  • Vissenberg K, Oyama M, Osato Y, Yokoyama R, Verbelen J-P, Nishitani K (2005a) Differential expression of AtXTH17, AtXTH18, AtXTH19 and AtXTH20 genes in Arabidopsis roots. Physiological roles in specification in cell wall construction. Plant Cell Physiol 46:192–200. DOI 10.1093/pcp/pci013

    Google Scholar 

  • Vissenberg K, Fry SC, Pauly M, Höfte H, Verbelen JP (2005b) XTH acts at the microfibril-matrix interface during cell elongation. J Exp Bot 56:673–683. DOI 10.1093/jxb/eri048

    Article  PubMed  Google Scholar 

  • Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383

    Article  PubMed  Google Scholar 

  • Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J (1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7:1555–1567

    Google Scholar 

  • Xu W, Campbell P, Vargheese AK, Braam J (1996) The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression. Plant J 9:879–889. DOI 10.1046/j.1365-313X.1996.9060879.x

    Article  PubMed  Google Scholar 

  • Yokoyama R, Nishitani K (2000) Functional diversity of xyloglucan-related proteins and its implications in the cell wall dynamics in plants. Plant Biol 2:598–604

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Yokoyama R, Nishitani K (2004) Genomic basis for cell-wall diversity in plants. A comparative approach to gene families in rice and Arabidopsis. Plant Cell Physiol 45:1111–1121. DOI 10.1093/pcp/pch151

    Google Scholar 

  • Yokoyama R, Rose JKC, Nishitani K (2004) A surprising diversity and abundance of xyloglucan endotransglucosylase/hydrolases in rice. Classification and expression analysis. Plant Physiol 134:1088–1099. DOI 10.1104/pp.103.035261

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas (17027001) and Scientific Research (B) (17370012) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and by the Program for “Development of Fundamental Technologies for Controlling the Process of Material Production of Plants” from the New Energy and Industrial Technology Development Organization, Japan.

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  1. Graduate School of Life Sciences, Tohoku University, Sendai, 980-8576, Japan

    Yasue Osato, Ryusuke Yokoyama & Kazuhiko Nishitani

  2. Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Sendai, 980-8578, Japan

    Kazuhiko Nishitani

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  1. Yasue Osato
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  2. Ryusuke Yokoyama
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Correspondence to Kazuhiko Nishitani.

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Osato, Y., Yokoyama, R. & Nishitani, K. A principal role for AtXTH18 in Arabidopsis thaliana root growth: a functional analysis using RNAi plants. J Plant Res 119, 153–162 (2006). https://doi.org/10.1007/s10265-006-0262-6

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