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ROOT GROWTH INHIBITING, a Rice Endo-1,4-β-d-Glucanase, Regulates Cell Wall Loosening and is Essential for Root Elongation

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Abstract

The molecular mechanism involved in cell wall dynamics has not been well clarified, although it is quite important for organ growth. We characterized a rice mutant, root growth inhibiting (rt), which is defective in root elongation. The rt mutant showed a severe defect in cell elongation at the root-elongating zone with additional collapse of epidermal and cortex cells at the root tip caused by the defect in the smooth exfoliation of root cap cells. Consistent with these phenotypes, expression of the RT gene, which encodes a member of the membrane-anchored endo-1,4-β-d-glucanase, was specifically localized in the root-elongating zone and at the junction between epidermal and root cap cells. The enzymatic analysis of root extracts from the wild-type and rt mutant indicated that RT hydrolyzes noncrystalline amorphous cellulose. The cellulose content was slightly increased but the crystallinity of cellulose was decreased in the rt root. In addition, the hemicellulose composition was different between wild-type and rt roots. The total extensibility was significantly lower in the rt root explants. Based on these results, we concluded that RT is involved in the disassembly of the cell wall for cell elongation in roots as well as for root cap exfoliation from the epidermal cell layer by hydrolyzing the noncrystalline amorphous cellulose fibers of cellulose microfibrils resulting in loosening of the hemicellulose and cellulose interaction.

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References

  • Beguin P (1990) Molecular biology of cellulose degradation. Annu Rev Microbiol 44:219–248

    Article  PubMed  CAS  Google Scholar 

  • Brummell DA, Catala C, Lashbrook CC, Bennett AB (1997) A membrane-anchored E-type endo-1,4-β-glucanase is localized on Golgi and plasma membranes of higher plants. Proc Natl Acad Sci USA 94:4794–4799

    Article  PubMed  CAS  Google Scholar 

  • Carpita NC (1996) Structure and biogenesis of the cell walls of grasses. Annu Rev Plant Physiol Plant Mol Biol 47:445–476

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2001) Wall structure and wall loosening. A look backwards and forwards. Plant Physiol 125:131–134

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  PubMed  CAS  Google Scholar 

  • Dale JE (1988) The control of leaf expansion. Ann Rev Plant Physiol Plant Mol Biol 39:267–295

    Article  Google Scholar 

  • del Campillo (1999) Multiple endo-1,4-β-d-glucanase (cellulase) genes in Arabidopsis. Curr Top Dev Biol 46:39–61

    Article  PubMed  CAS  Google Scholar 

  • del Campillo E, Bennett AB (1996) Pedicel breakstrength and cellulase gene expression during tomato flower abscission. Plant Physiol 111:813–820

    Article  PubMed  CAS  Google Scholar 

  • del Campillo E, Lewis LN (1992) Occurrence of 9.5 cellulase and other hydrolases in flower reproductive organs undergoing major cell wall disruption. Plant Physiol 99:1015–1020

    Article  PubMed  CAS  Google Scholar 

  • del Campillo E, Abdel-Aziz A, Crawford D, Patterson SE (2004) Root cap specific expression of an endo-β-1,4-d-glucanase (cellulase): a new marker to study root development in Arabidopsis. Plant Mol Biol 56:309–323

    Article  PubMed  CAS  Google Scholar 

  • Futsuhara Y, Kitano H (1985) Inheritance of a root-growth inhibiting mutant in rice. Rice Genet Newslett 2:70–71

    Google Scholar 

  • Gonzalez-Bosch C, del Campillo E, Bennett AB (1997) Immunodetection and characterization of tomato endo-β-1,4-glucanase cel1 protein in flower abscission zones. Plant Physiol 114:1541–1546

    Article  PubMed  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of boundaries of the T-DNA. Plant J 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • His I, Driouich A, Nicol F, Jauneau A, Hofte H (2001) Altered pectin composition in primary cell walls of korrigan, a dwarf mutant of Arabidopsis deficient in a membrane-bound endo-1,4-β-glucanase. Planta 212:348–358

    Article  PubMed  CAS  Google Scholar 

  • Kutschera U (1992) The role of the epidermis in the control of elongation growth in stems and coleoptiles. Bot Acta 105:246–252

    Google Scholar 

  • Lane DR, Wiedemeier A, Peng L, Hofte H, Vernhettes S, Desprez T, Hocart CH, Birch RJ, Baskin TI, Burn JE, Arioli T, Betzner AS, Williamson RE (2001) Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol 126:278–288

    Article  PubMed  CAS  Google Scholar 

  • Lashbrook CC, Gonzalez-Bosch C, Bennett AB (1994) Two divergent endo-β-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell 6:1485–1493

    PubMed  CAS  Google Scholar 

  • Levy I, Shani Z, Shoseyov O (2002) Modification of polysaccharides and plant cell wall by endo-1,4-β-glucanase and cellulose-binding domains. Biomol Eng 19:17–30

    Article  PubMed  CAS  Google Scholar 

  • Libertini E, Li Y, McQueen-Mason SJ (2004) Phylogenetic analysis of the plant endo-β-1,4-glucanase gene family. J Mol Evol 58:506–515

    Article  PubMed  CAS  Google Scholar 

  • Milioni D, Sado PE, Stacey NJ, Domingo C, Roberts K, McCann MC (2001) Differential expression of cell-wall-related genes during the formation of tracheary elements in the Zinnia mesophyll cell system. Plant Mol Biol 47:221–238

    Article  PubMed  CAS  Google Scholar 

  • Milioni D, Sado PE, Stacey NJ, Roberts K, McCann MC (2002) Early gene expression associated with the commitment and differentiation of a plant tracheary element is revealed by cDNA-amplified fragment length polymorphism analysis. Plant Cell 14:2813–2824

    Article  PubMed  CAS  Google Scholar 

  • Mφlhφj M, Jorgensen B, Ulvskov P, Borkhardt B (2001a) Two Arabidopsis thaliana genes, KOR2 and KOR3, which encode membrane-anchored endo-1,4-β-d-glucanases, are differentially expressed in developing leaf trichomes and their support cells. Plant Mol Biol 46:263–275

    Article  Google Scholar 

  • Mφlhφj M, Ulvskov P, Dal Degan F (2001b) Characterization of a functional soluble form of a Brassica napus membrane-anchored endo-1,4-β-glucanase heterologously expressed in Pichia pastoris. Plant Physiol 127:674–684

    Article  Google Scholar 

  • Nakagawa N, Sakurai N (1998) Increase in the amount of celA1 protein in tobacco BY-2 cells by a cellulose biosynthesis inhibitor, 2,6-dichlorobenzonitrile. Plant Cell Physiol 39:779–785

    Article  PubMed  CAS  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Hofte H (1998) A plasma membrane-bound putative endo-1,4-β-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576

    Article  PubMed  CAS  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    PubMed  CAS  Google Scholar 

  • Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J 33:1099–1106

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Kawagoe Y, Hogan P, Delmer D (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295:147–150

    Article  PubMed  CAS  Google Scholar 

  • Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1,4-β-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263

    Article  PubMed  CAS  Google Scholar 

  • Savaldi-Goldstein S, Peto C, Chory J (2007) The epidermis both drives and restricts plant shoot growth. Nature 446:199–202

    Article  PubMed  CAS  Google Scholar 

  • Segal L, Creely JJ, Martin AE, Conrad CM (1959) An empirical method for estimating the degree of crystallinity of native cellulose using the X-ray diffractometer. Text Res J 29:786–794

    Article  CAS  Google Scholar 

  • Shedletzky E, Shmuel M, Delmer DP, Lamport DT (1990) Adaptation and growth of tomato cells on the herbicide 2,6-dichlorobenzonitrile leads to production of unique cell walls virtually lacking a cellulose-xyloglucan network. Plant Physiol 94:980–987

    Article  PubMed  CAS  Google Scholar 

  • Takahashi J, Rudsander UJ, Hedenström M, Banasiak A, Harholt J, Amelot N, Immerzeel P, Ryden P, Endo S, Ibatullin FM, Brumer H, del Campillo E, Master ER, Scheller HV, Sundberg B, Teeri TT, Mellerowicz EJ (2009) KORRIGAN1 and its aspen homolog PttCel9A1 decrease cellulose crystallinity in Arabidopsis stems. Plant Cell Physiol 50:1099–1115

    Article  PubMed  CAS  Google Scholar 

  • Tanimoto E, Fujii S, Yamamoto R, Inagana S (2000) Measurement of viscoelastic properties of root cell walls affected by low pH in lateral roots of Pisum sativum L. Plant Soil 226:21–28

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tucker ML, Sexton R, del Campillo E, Lewis LN (1988) Bean abscission cellulase: characterization of a cDNA clone and regulation of gene expression by ethylene and auxin. Plant Physiol 88:1257–1262

    Article  PubMed  CAS  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    PubMed  CAS  Google Scholar 

  • Zhou HL, He SJ, Cao YR, Chen T, Du BX, Chu CC, Zhang JS, Chen SY (2006) OsGLU1, a putative membrane-bound endo-1,4-β-d-glucanase from rice, affects plant internode elongation. Plant Mol Biol 60:137–151

    Article  PubMed  CAS  Google Scholar 

  • Zuo J, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH (2000) KORRIGAN, an arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12:1137–1152

    PubMed  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi, 464-8601, Japan

    Yoshiaki Inukai, Masami Miwa, Miho Kojima & Hiroyuki Yamamoto

  2. Faculty of Bioresources and Environmental Sciences, Ishikawa Prefectural University, Nonoichi, Ishikawa, 921-8836, Japan

    Tomoaki Sakamoto

  3. Bioscience and Biotechnology Center, Nagoya University, Nagoya, Aichi, 464-8601, Japan

    Yoichi Morinaka, Makoto Matsuoka & Hidemi Kitano

  4. Graduate School of Natural Sciences, Nagoya City University, Nagoya, Aichi, 467-8501, Japan

    Eiichi Tanimoto

  5. Graduate School of Bio-Applications & Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, Tokyo, 184-8588, Japan

    Kanna Sato & Yoshihiro Katayama

Authors
  1. Yoshiaki Inukai
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  2. Tomoaki Sakamoto
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  3. Yoichi Morinaka
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  4. Masami Miwa
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  5. Miho Kojima
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  6. Eiichi Tanimoto
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  7. Hiroyuki Yamamoto
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  8. Kanna Sato
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  9. Yoshihiro Katayama
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  10. Makoto Matsuoka
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  11. Hidemi Kitano
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Correspondence to Tomoaki Sakamoto.

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Inukai, Y., Sakamoto, T., Morinaka, Y. et al. ROOT GROWTH INHIBITING, a Rice Endo-1,4-β-d-Glucanase, Regulates Cell Wall Loosening and is Essential for Root Elongation. J Plant Growth Regul 31, 373–381 (2012). https://doi.org/10.1007/s00344-011-9247-3

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  • DOI: https://doi.org/10.1007/s00344-011-9247-3

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