Skip to main content
SpringerLink
Log in

AtCYT-INV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Neutral/Alkaline invertases are unique to plant and photosynthetic bacteria. The function of Neutral/Alkaline invertases in plant development is not clear so far. In this study, we isolated an Arabidopsis (Col-0) mutant insensitive to osmotic stress-induced inhibition on lateral root growth. Map-based cloning reveals that a neutral invertase gene (AtCYT-INV1) was point-mutated. The mutant Atcyt-inv1 showed short primary root, smaller size of leaves and siliques, and promotion of the reproductive compared to the wild type (WT). Carbohydrate measurement showed that sucrose is accumulated and glucose is reduced in the mutant Atcyt-inv1 under normal and 3% mannitol treatments. Taken together, AtCYT-INV1 plays multiple roles in plant development and is involved in osmotic stress-induced inhibition on lateral root growth by controlling the concentration of hexose in cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, León P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 14:2085–2096

    PubMed  CAS  Google Scholar 

  • Bradford M (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

    Article  Google Scholar 

  • Brocard IM, Lynch TJ, Finkelstein RR (2002) Regulation and role of the arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiol 129:1533–1543

    Article  PubMed  CAS  Google Scholar 

  • Chen Y, Ji FF, Xie H, Liang JS, Zhang JH (2006) The regulator of G-protein signaling proteins involved in sugar and abscisic acid siganling in Arabidopsis seed geimination. Plant Physiol 140:302–310

    Article  PubMed  CAS  Google Scholar 

  • Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743

    Article  PubMed  CAS  Google Scholar 

  • Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  PubMed  Google Scholar 

  • Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43:17–28

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gibson SI (2001) ABA and sugar interactions regulating development: cross-talk or voices in a crowd? Curr Opin Plant Biol 5:26–32

    Article  Google Scholar 

  • Gallagher JA, Pollock CJ (1998) Isolation and characterization of a cDNA clone from Lolium temulentum L. encoding for a sucrose hydrolytic enzyme which shows alkaline/neutral invertase activity. J Exp Bot 49:789–795

    Article  CAS  Google Scholar 

  • Heyer AG, Raap M, Schroeer B, Marty B, Willmitzer L (2004) Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. Plant J 39:161–169

    Article  PubMed  CAS  Google Scholar 

  • Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Schinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333

    Article  PubMed  CAS  Google Scholar 

  • Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487

    Article  CAS  Google Scholar 

  • Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato fruit. Plant Physiol 103:863–870

    PubMed  CAS  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  PubMed  CAS  Google Scholar 

  • Kühn C, Barker L, Bürkle L, Frommer WB (1999) Update on sucrose transport in higher plants. J Exp Bot 50:935–953

    Article  Google Scholar 

  • Lee HS, Sturm A (1996) Purification and characterization of neutral and alkaline invertase from carrot. Plant Physiol 112:1513–1522

    Article  PubMed  CAS  Google Scholar 

  • León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116

    Article  PubMed  CAS  Google Scholar 

  • Lou Y, Gou JY, Xue HW (2007) PIP5K9, and Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181

    Article  PubMed  CAS  Google Scholar 

  • Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77

    Article  PubMed  CAS  Google Scholar 

  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signalling. Science 300:332–336

    Article  PubMed  CAS  Google Scholar 

  • Murayama S, Handa H (2007) Genes for alkaline/neutral invertase in rice: alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 225:1193–1203

    Article  PubMed  CAS  Google Scholar 

  • Pelah D, Wang W, Altman A, Shoseyov O, Bartels D (1997) Differential accumulation of water stress-related proteins, sucrose synthase and soluble sugars in Populus species that differ in their water stress response. Physiol Plant 99:153–159

    Article  CAS  Google Scholar 

  • Roldán M, Gómez-Mena C, Ruiz-García L, Salinas J, Martínez-Zapater M (1999) Sucrose availability on the aerial part of the plant promotes morphogenesis and flowering of Arabidopsis in the dark. Plant J 20:581–590

    Article  PubMed  Google Scholar 

  • Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell 14:S185–S205

    Google Scholar 

  • Rook F, Corke F, Card R, Munz G, Smith C, Bevan MW (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling. Plant J 26:421–433

    Article  PubMed  CAS  Google Scholar 

  • Rook F, Gerrits N, Kortstee A, Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signaling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15:253–263

    Article  PubMed  CAS  Google Scholar 

  • Sergeeva LI, Keurentjes JJB, Bentsink L, Vonk J, van der Plas LKW, Koornneef M, Vreugdenhil D (2006) Vacuolar invertase regulate elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc Natl Acad Sci USA 103:2994–2999

    Article  PubMed  CAS  Google Scholar 

  • Signora L, Smet ID, Foyer CH, Zhang H (2001) ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J 28:655–662

    Article  PubMed  CAS  Google Scholar 

  • Smet ID, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555

    Article  PubMed  Google Scholar 

  • Sonnewald U, Brauer M, Schaewen A, Stitt M, Willmitzer L (1991) Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J 1:95–106

    Article  PubMed  CAS  Google Scholar 

  • Sturm A (1999) Invertase. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7

    Article  PubMed  CAS  Google Scholar 

  • Tang GQ, Luscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11:177–189

    Article  PubMed  CAS  Google Scholar 

  • Valentovič P, Luxová M, Kolarovič L, Gašparíková O (2006) Effect of osmotic stress on compatible solutes content, membrane stability and water relations in two maize cultivars. Plant Soil Environ 52:186–191

    Google Scholar 

  • Vargas W, Cumino A, Salerno GL (2003) Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol? Planta 216:951–960

    PubMed  CAS  Google Scholar 

  • Weber H, Heim U, Golombek S, Borisjuk L, Manteuffel R, Wobus U (1998) Expression of a yeast-derived invertase in developing cotyledons of Vicia narbonensis alters the carbohydrate state and affects storage functions. Plant J 16:163–172

    Article  PubMed  CAS  Google Scholar 

  • Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis. J Biol Chem 277:8588–8596

    Article  PubMed  CAS  Google Scholar 

  • Ye GN, Stone D, Pang SZ, Creely W, Gonzalez K, Hinchee M (1999) Arabidopsis ovule is the target for Agrobacterium in planta vacuum infiltration transformation. Plant J 19:249–257

    Article  PubMed  Google Scholar 

  • Zrenner R, Schuler K, Sonnewald U (1996) Soluble acid invertase determines the hexose-to-sucrose ratio in cold-stored potato tubers. Planta 198:246–252

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr Peter Doerner for generous gifts of the transgenic Arabidopsis seeds expressing CycB1 promoter-GUS. This research was supported by the National Basic Research Program of China (973) (No. 2005CB120901).

Author information

Authors and Affiliations

  1. The State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, 310058, PR China

    Xiaopeng Qi, Zhongchang Wu, Jinhui Li, Xiaorong Mo, Shihua Wu, Jun Chu & Ping Wu

Authors
  1. Xiaopeng Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongchang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinhui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaorong Mo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shihua Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jun Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ping Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ping Wu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 324 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Qi, X., Wu, Z., Li, J. et al. AtCYT-INV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis . Plant Mol Biol 64, 575–587 (2007). https://doi.org/10.1007/s11103-007-9177-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-007-9177-4

Keywords

Search

Navigation