DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa

Abstract

In higher plants, cell wall invertase (CWI) and vacuolar invertase (VI) were considered to be essential coordinators in carbohydrate partitioning, sink strength determination, and stress responses. An increasing body of evidence revealed that the tight regulation of CWI and VI substantially depends on the post-translational mechanisms, which were mediated by small proteinaceous inhibitors (C/VIFs, Inhibitor of β-Fructosidases). As yet, the extensive survey of the molecular basis and biochemical property of C/VIFs remains largely unknown in black cottonwood (Populus trichocarpa Torr. & A. Gray), a model species of woody plants. In the present work, we have initiated a systematic review of the genomic structures, phylogenies, cis-regulatory elements, and conserved motifs as well as the tissue-specific expression, resulting in the identification of 39 genes encoding C/VIF in poplar genome. We characterized two putative invertase inhibitors PtC/VIF1 and 2, showing predominant transcript levels in the roots and highly divergent responses to the selected stress cues including fusarium wilt, drought, ABA, wound, and senescence. In silico prediction of the signal peptide hinted us that they both likely had the apoplastic targets. Based on the experimental visualization via the transient and stable transformation assays, we confirmed that PtC/VIF1 and 2 indeed secreted to the extracellularmore » compartments. Further validation of their recombinant enzymes revealed that they displayed the potent inhibitory affinities on the extracted CWI, supporting the patterns that act as the typical apoplastic invertase inhibitors. To our knowledge, it is the first report on molecular characterization of the functional C/VIF proteins in poplar. Our results indicate that PtC/VIF1 and 2 may exert essential roles in defense- and stress-related responses. Moreover, novel findings of the up- and downregulated C/VIF genes and functional enzyme activities enable us to further unravel the molecular mechanisms in the promotion of woody plant performance and adapted-biotic stress, underlying the homeostatic control of sugar in the apoplast.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Nanjing Forestry Univ. (China)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Natural Science Foundation of China (NSFC); Natural ScienceFoundation of Jiangsu Province (NSFJ); Scientific Research Foundation for High-Level Talents of Nanjing Forestry University (SRFNFU); Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD)
OSTI Identifier:
1628299
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 10; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; plant sciences; poplar, invertase inhibitor, sucrose, apoplast, pathogen, defense response, drought

Citation Formats

Su, Tao, Han, Mei, Min, Jie, Zhou, Huaiye, Zhang, Qi, Zhao, Jingyi, and Fang, Yanming. Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa. United States: N. p., 2020. Web. doi:10.3389/fpls.2019.01654.
Su, Tao, Han, Mei, Min, Jie, Zhou, Huaiye, Zhang, Qi, Zhao, Jingyi, & Fang, Yanming. Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa. United States. https://doi.org/10.3389/fpls.2019.01654
Su, Tao, Han, Mei, Min, Jie, Zhou, Huaiye, Zhang, Qi, Zhao, Jingyi, and Fang, Yanming. Wed . "Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa". United States. https://doi.org/10.3389/fpls.2019.01654. https://www.osti.gov/servlets/purl/1628299.
@article{osti_1628299,
title = {Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa},
author = {Su, Tao and Han, Mei and Min, Jie and Zhou, Huaiye and Zhang, Qi and Zhao, Jingyi and Fang, Yanming},
abstractNote = {In higher plants, cell wall invertase (CWI) and vacuolar invertase (VI) were considered to be essential coordinators in carbohydrate partitioning, sink strength determination, and stress responses. An increasing body of evidence revealed that the tight regulation of CWI and VI substantially depends on the post-translational mechanisms, which were mediated by small proteinaceous inhibitors (C/VIFs, Inhibitor of β-Fructosidases). As yet, the extensive survey of the molecular basis and biochemical property of C/VIFs remains largely unknown in black cottonwood (Populus trichocarpa Torr. & A. Gray), a model species of woody plants. In the present work, we have initiated a systematic review of the genomic structures, phylogenies, cis-regulatory elements, and conserved motifs as well as the tissue-specific expression, resulting in the identification of 39 genes encoding C/VIF in poplar genome. We characterized two putative invertase inhibitors PtC/VIF1 and 2, showing predominant transcript levels in the roots and highly divergent responses to the selected stress cues including fusarium wilt, drought, ABA, wound, and senescence. In silico prediction of the signal peptide hinted us that they both likely had the apoplastic targets. Based on the experimental visualization via the transient and stable transformation assays, we confirmed that PtC/VIF1 and 2 indeed secreted to the extracellular compartments. Further validation of their recombinant enzymes revealed that they displayed the potent inhibitory affinities on the extracted CWI, supporting the patterns that act as the typical apoplastic invertase inhibitors. To our knowledge, it is the first report on molecular characterization of the functional C/VIF proteins in poplar. Our results indicate that PtC/VIF1 and 2 may exert essential roles in defense- and stress-related responses. Moreover, novel findings of the up- and downregulated C/VIF genes and functional enzyme activities enable us to further unravel the molecular mechanisms in the promotion of woody plant performance and adapted-biotic stress, underlying the homeostatic control of sugar in the apoplast.},
doi = {10.3389/fpls.2019.01654},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {United States},
year = {Wed Jan 08 00:00:00 EST 2020},
month = {Wed Jan 08 00:00:00 EST 2020}
}

Works referenced in this record:

Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato
journal, November 2014

  • Albacete, Alfonso; Cantero-Navarro, Elena; Großkinsky, Dominik K.
  • Journal of Experimental Botany, Vol. 66, Issue 3
  • DOI: 10.1093/jxb/eru448

Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development
journal, June 2004


Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean ( Glycine max )
journal, December 2016


Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors
journal, December 2008

  • Wilkins, Olivia; Nahal, Hardeep; Foong, Justin
  • Plant Physiology, Vol. 149, Issue 2
  • DOI: 10.1104/pp.108.132795

Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana
journal, April 2018

  • Barnes, William J.; Anderson, Charles T.
  • The Plant Journal, Vol. 94, Issue 6
  • DOI: 10.1111/tpj.13909

Regulation of assimilate import into sink organs: update on molecular drivers of sink strength
journal, January 2013

  • Bihmidine, Saadia; Hunter, Charles T.; Johns, Christine E.
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00177

Genetic Evidence for the Role of a Rice Vacuolar Invertase as a Molecular Sink Strength Determinant
journal, January 2018


RNA Interference-Mediated Repression of Cell Wall Invertase Impairs Defense in Source Leaves of Tobacco
journal, May 2008

  • Essmann, Jutta; Schmitz-Thom, Ina; Schön, Hardy
  • Plant Physiology, Vol. 147, Issue 3
  • DOI: 10.1104/pp.108.121418

Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009

  • Coleman, H. D.; Yan, J.; Mansfield, S. D.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
  • DOI: 10.1073/pnas.0900188106

MEME: discovering and analyzing DNA and protein sequence motifs
journal, July 2006

  • Bailey, T. L.; Williams, N.; Misleh, C.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl198

Control of rice grain-filling and yield by a gene with a potential signature of domestication
journal, September 2008

  • Wang, Ertao; Wang, Jianjun; Zhu, Xudong
  • Nature Genetics, Vol. 40, Issue 11
  • DOI: 10.1038/ng.220

Tolerance to drought and salt stress in plants: Unraveling the signaling networks
journal, April 2014


Reassessment of an Arabidopsis cell wall invertase inhibitor AtCIF1 reveals its role in seed germination and early seedling growth
journal, November 2015


Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew
journal, June 2006


Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses: Cell-wall invertase in the defence response
journal, May 2014

  • Proels, Reinhard Korbinian; Hückelhoven, Ralph
  • Molecular Plant Pathology, Vol. 15, Issue 8
  • DOI: 10.1111/mpp.12139

Populus : A Model System for Plant Biology
journal, June 2007


Extracellular Invertase Is an Essential Component of Cytokinin-Mediated Delay of Senescence
journal, April 2004

  • Balibrea Lara, Maria Encarnación; Gonzalez Garcia, Maria-Cruz; Fatima, Tahira
  • The Plant Cell, Vol. 16, Issue 5
  • DOI: 10.1105/tpc.018929

Evolution and diversity of invertase genes in Populus trichocarpa
journal, October 2007


Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana
journal, March 2011

  • Xiang, Li; Le Roy, Katrien; Bolouri-Moghaddam, Mohammad-Reza
  • Journal of Experimental Botany, Vol. 62, Issue 11
  • DOI: 10.1093/jxb/err069

A Tomato Vacuolar Invertase Inhibitor Mediates Sucrose Metabolism and Influences Fruit Ripening
journal, September 2016

  • Qin, Guozheng; Zhu, Zhu; Wang, Weihao
  • Plant Physiology, Vol. 172, Issue 3
  • DOI: 10.1104/pp.16.01269

A gain-of-function mutation of plastidic invertase alters nuclear gene expression with sucrose treatment partially via GENOMES UNCOUPLED1-mediated signaling
journal, January 2015

  • Maruta, Takanori; Miyazaki, Nozomi; Nosaka, Ryota
  • New Phytologist, Vol. 206, Issue 3
  • DOI: 10.1111/nph.13309

Plant–Pathogen Maneuvering over Apoplastic Sugars
journal, September 2017


Ectopic expression of a tobacco vacuolar invertase inhibitor in guard cells confers drought tolerance in Arabidopsis
journal, February 2016

  • Chen, Su-Fen; Liang, Ke; Yin, Dong-Mei
  • Journal of Enzyme Inhibition and Medicinal Chemistry, Vol. 31, Issue 6
  • DOI: 10.3109/14756366.2016.1142981

An Invertase Inhibitor from Maize Localizes to the Embryo Surrounding Region during Early Kernel Development
journal, December 2003

  • Bate, Nicholas J.; Niu, Xiping; Wang, Yuwen
  • Plant Physiology, Vol. 134, Issue 1
  • DOI: 10.1104/pp.103.027466

GSDS 2.0: an upgraded gene feature visualization server
journal, December 2014


Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond
journal, February 2018


Plant protein inhibitors of invertases
journal, February 2004

  • Rausch, Thomas; Greiner, Steffen
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1696, Issue 2
  • DOI: 10.1016/j.bbapap.2003.09.017

Simple, rapid and efficient transformation of genotype Nisqually-1: a basic tool for the first sequenced model tree
journal, June 2017


Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers
journal, July 1999

  • Greiner, Steffen; Rausch, Thomas; Sonnewald, Uwe
  • Nature Biotechnology, Vol. 17, Issue 7
  • DOI: 10.1038/10924

An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth
journal, April 2006


Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis
journal, February 2006

  • Sergeeva, L. I.; Keurentjes, J. J. B.; Bentsink, L.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 8
  • DOI: 10.1073/pnas.0511015103

The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata
journal, January 2019

  • Wei, Tonglu; Wang, Yue; Xie, Zongzhou
  • Plant Biotechnology Journal, Vol. 17, Issue 7
  • DOI: 10.1111/pbi.13064

StInvInh2 as an inhibitor of StvacINV1 regulates the cold-induced sweetening of potato tubers by specifically capping vacuolar invertase activity
journal, February 2013

  • Liu, Xun; Lin, Yuan; Liu, Jun
  • Plant Biotechnology Journal, Vol. 11, Issue 5
  • DOI: 10.1111/pbi.12054

Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit development
journal, June 2008

  • Yu, X.; Wang, X.; Zhang, W.
  • Journal of Experimental Botany, Vol. 59, Issue 11
  • DOI: 10.1093/jxb/ern158

In Arabidopsis thaliana , the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles
journal, August 2004


A 6&1-FEH Encodes an Enzyme for Fructan Degradation and Interact with Invertase Inhibitor Protein in Maize (Zea mays L.)
journal, August 2019

  • Zhao, Hongbo; Greiner, Steffen; Scheffzek, Klaus
  • International Journal of Molecular Sciences, Vol. 20, Issue 15
  • DOI: 10.3390/ijms20153807

Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana: Invertase and clubroot disease
journal, October 2010


Sucrose and invertases, a part of the plant defense response to the biotic stresses
journal, June 2014


Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein
journal, September 2010

  • Hothorn, M.; Van den Ende, W.; Lammens, W.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
  • DOI: 10.1073/pnas.1004481107

Genome-Wide Survey of Invertase Encoding Genes and Functional Characterization of an Extracellular Fungal Pathogen-Responsive Invertase in Glycine max
journal, August 2018

  • Su, Tao; Han, Mei; Min, Jie
  • International Journal of Molecular Sciences, Vol. 19, Issue 8
  • DOI: 10.3390/ijms19082395

Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants
journal, March 2011

  • Brummell, David A.; Chen, Ronan K. Y.; Harris, John C.
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err043

Cytosolic invertase contributes to the supply of substrate for cellulose biosynthesis in developing wood
journal, December 2016

  • Rende, Umut; Wang, Wei; Gandla, Madhavi Latha
  • New Phytologist, Vol. 214, Issue 2
  • DOI: 10.1111/nph.14392

Genetic control of cell wall invertases in developing endosperm of maize
journal, July 2005


Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes: Donor and acceptor substrate selectivity in GH32
journal, September 2009


MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

Sugar transporters in plants and in their interactions with fungi
journal, July 2012


Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
journal, June 2002


SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006


Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998


Vacuolar sucrose cleavage prevents limitation of cytosolic carbohydrate metabolism and stabilizes photosynthesis under abiotic stress
journal, September 2018

  • Weiszmann, Jakob; Fürtauer, Lisa; Weckwerth, Wolfram
  • The FEBS Journal, Vol. 285, Issue 21
  • DOI: 10.1111/febs.14656

Constitutive expression of cell wall invertase genes increases grain yield and starch content in maize
journal, August 2013

  • Li, Bei; Liu, Hua; Zhang, Yue
  • Plant Biotechnology Journal, Vol. 11, Issue 9
  • DOI: 10.1111/pbi.12102

Silencing of vacuolar invertase and asparagine synthetase genes and its impact on acrylamide formation of fried potato products
journal, June 2015

  • Zhu, Xiaobiao; Gong, Huiling; He, Qunyan
  • Plant Biotechnology Journal, Vol. 14, Issue 2
  • DOI: 10.1111/pbi.12421

Cloning of a Tobacco Apoplasmic Invertase Inhibitor: Proof of Function of the Recombinant Protein and Expression Analysis during Plant Development
journal, February 1998

  • Greiner, Steffen; Krausgrill, Silke; Rausch, Thomas
  • Plant Physiology, Vol. 116, Issue 2
  • DOI: 10.1104/pp.116.2.733

Antisense Acid Invertase (TIV1) Gene Alters Soluble Sugar Composition and Size in Transgenic Tomato Fruit
journal, November 1996


Extracellular invertase: key metabolic enzyme and PR protein
journal, January 2003

  • Roitsch, T.; Balibrea, M. E.; Hofmann, M.
  • Journal of Experimental Botany, Vol. 54, Issue 382
  • DOI: 10.1093/jxb/erg050

Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling
journal, April 2014


Functional Characterization of a Drought-Responsive Invertase Inhibitor from Maize (Zea mays L.)
journal, August 2019

  • Chen, Lin; Liu, Xiaohong; Huang, Xiaojia
  • International Journal of Molecular Sciences, Vol. 20, Issue 17
  • DOI: 10.3390/ijms20174081

Prolonged Expression of a Putative Invertase Inhibitor in Micropylar Endosperm Suppressed Embryo Growth in Arabidopsis
journal, January 2018


Targeting the AtCWIN1 Gene to Explore the Role of Invertases in Sucrose Transport in Roots and during Botrytis cinerea Infection
journal, December 2016

  • Veillet, Florian; Gaillard, Cécile; Coutos-Thévenot, Pierre
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.01899

Suppression of the Vacuolar Invertase Gene Prevents Cold-Induced Sweetening in Potato
journal, August 2010

  • Bhaskar, Pudota B.; Wu, Lei; Busse, James S.
  • Plant Physiology, Vol. 154, Issue 2
  • DOI: 10.1104/pp.110.162545

A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection
journal, July 2017

  • Chang, Qing; Liu, Jie; Lin, Xiaohong
  • New Phytologist, Vol. 215, Issue 4
  • DOI: 10.1111/nph.14666

Aberrant seed development in Litchi chinensis is associated with the impaired expression of cell wall invertase genes
journal, August 2018


Invertases. Primary Structures, Functions, and Roles in Plant Development and Sucrose Partitioning
journal, September 1999


The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato
journal, November 2017


Structural Insights into the Target Specificity of Plant Invertase and Pectin Methylesterase Inhibitory Proteins
journal, November 2004

  • Hothorn, Michael; Wolf, Sebastian; Aloy, Patrick
  • The Plant Cell, Vol. 16, Issue 12
  • DOI: 10.1105/tpc.104.025684

Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato
journal, May 2015

  • Albacete, A.; Cantero-Navarro, E.; Grosskinsky, D. K.
  • Journal of Experimental Botany, Vol. 66, Issue 11
  • DOI: 10.1093/jxb/erv134

CsINV5, a tea vacuolar invertase gene enhances cold tolerance in transgenic Arabidopsis
journal, October 2018


Point Mutation of a Plastidic Invertase Inhibits Development of the Photosynthetic Apparatus and Enhances Nitrate Assimilation in Sugar-treated Arabidopsis Seedlings
journal, March 2010

  • Tamoi, Masahiro; Tabuchi, Tomoki; Demuratani, Masayo
  • Journal of Biological Chemistry, Vol. 285, Issue 20
  • DOI: 10.1074/jbc.M109.055111

Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis
journal, November 2003


An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020


Genetic control of cell wall invertases in developing endosperm of maize
journal, July 2005


In Arabidopsis thaliana , the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles
journal, August 2004


Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development
journal, June 2004


Sugar transporters in plants and in their interactions with fungi
journal, July 2012


Plant–Pathogen Maneuvering over Apoplastic Sugars
journal, September 2017


Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond
journal, February 2018


Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers
journal, July 1999

  • Greiner, Steffen; Rausch, Thomas; Sonnewald, Uwe
  • Nature Biotechnology, Vol. 17, Issue 7
  • DOI: 10.1038/10924

Aberrant seed development in Litchi chinensis is associated with the impaired expression of cell wall invertase genes
journal, August 2018


Influence of cluster thinning and girdling on aroma composition in ‘Jumeigui’ table grape
journal, April 2020


Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans
journal, February 2022


Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis
journal, February 2006

  • Sergeeva, L. I.; Keurentjes, J. J. B.; Bentsink, L.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 8
  • DOI: 10.1073/pnas.0511015103

Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure
journal, July 2009

  • Coleman, H. D.; Yan, J.; Mansfield, S. D.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 31
  • DOI: 10.1073/pnas.0900188106

Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein
journal, September 2010

  • Hothorn, M.; Van den Ende, W.; Lammens, W.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
  • DOI: 10.1073/pnas.1004481107

GSDS 2.0: an upgraded gene feature visualization server
journal, December 2014


Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit development
journal, June 2008

  • Yu, X.; Wang, X.; Zhang, W.
  • Journal of Experimental Botany, Vol. 59, Issue 11
  • DOI: 10.1093/jxb/ern158

Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants
journal, March 2011

  • Brummell, David A.; Chen, Ronan K. Y.; Harris, John C.
  • Journal of Experimental Botany, Vol. 62, Issue 10
  • DOI: 10.1093/jxb/err043

Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana
journal, March 2011

  • Xiang, Li; Le Roy, Katrien; Bolouri-Moghaddam, Mohammad-Reza
  • Journal of Experimental Botany, Vol. 62, Issue 11
  • DOI: 10.1093/jxb/err069

Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato
journal, November 2014

  • Albacete, Alfonso; Cantero-Navarro, Elena; Großkinsky, Dominik K.
  • Journal of Experimental Botany, Vol. 66, Issue 3
  • DOI: 10.1093/jxb/eru448

Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean ( Glycine max )
journal, December 2016


MEME: discovering and analyzing DNA and protein sequence motifs
journal, July 2006

  • Bailey, T. L.; Williams, N.; Misleh, C.
  • Nucleic Acids Research, Vol. 34, Issue Web Server
  • DOI: 10.1093/nar/gkl198

An Invertase Inhibitor from Maize Localizes to the Embryo Surrounding Region during Early Kernel Development
journal, December 2003

  • Bate, Nicholas J.; Niu, Xiping; Wang, Yuwen
  • Plant Physiology, Vol. 134, Issue 1
  • DOI: 10.1104/pp.103.027466

RNA Interference-Mediated Repression of Cell Wall Invertase Impairs Defense in Source Leaves of Tobacco
journal, May 2008

  • Essmann, Jutta; Schmitz-Thom, Ina; Schön, Hardy
  • Plant Physiology, Vol. 147, Issue 3
  • DOI: 10.1104/pp.108.121418

Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors
journal, December 2008

  • Wilkins, Olivia; Nahal, Hardeep; Foong, Justin
  • Plant Physiology, Vol. 149, Issue 2
  • DOI: 10.1104/pp.108.132795

Suppression of the Vacuolar Invertase Gene Prevents Cold-Induced Sweetening in Potato
journal, August 2010

  • Bhaskar, Pudota B.; Wu, Lei; Busse, James S.
  • Plant Physiology, Vol. 154, Issue 2
  • DOI: 10.1104/pp.110.162545

Antisense Acid Invertase (TIV1) Gene Alters Soluble Sugar Composition and Size in Transgenic Tomato Fruit
journal, November 1996


Cloning of a Tobacco Apoplasmic Invertase Inhibitor: Proof of Function of the Recombinant Protein and Expression Analysis during Plant Development
journal, February 1998

  • Greiner, Steffen; Krausgrill, Silke; Rausch, Thomas
  • Plant Physiology, Vol. 116, Issue 2
  • DOI: 10.1104/pp.116.2.733

A Tomato Vacuolar Invertase Inhibitor Mediates Sucrose Metabolism and Influences Fruit Ripening
journal, September 2016

  • Qin, Guozheng; Zhu, Zhu; Wang, Weihao
  • Plant Physiology, Vol. 172, Issue 3
  • DOI: 10.1104/pp.16.01269

Extracellular Invertase Is an Essential Component of Cytokinin-Mediated Delay of Senescence
journal, April 2004

  • Balibrea Lara, Maria Encarnación; Gonzalez Garcia, Maria-Cruz; Fatima, Tahira
  • The Plant Cell, Vol. 16, Issue 5
  • DOI: 10.1105/tpc.018929

Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew
journal, June 2006


An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth
journal, April 2006


Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes: Donor and acceptor substrate selectivity in GH32
journal, September 2009


Cytosolic invertase contributes to the supply of substrate for cellulose biosynthesis in developing wood
journal, December 2016

  • Rende, Umut; Wang, Wei; Gandla, Madhavi Latha
  • New Phytologist, Vol. 214, Issue 2
  • DOI: 10.1111/nph.14392

A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection
journal, July 2017

  • Chang, Qing; Liu, Jie; Lin, Xiaohong
  • New Phytologist, Vol. 215, Issue 4
  • DOI: 10.1111/nph.14666

StInvInh2 as an inhibitor of StvacINV1 regulates the cold-induced sweetening of potato tubers by specifically capping vacuolar invertase activity
journal, February 2013

  • Liu, Xun; Lin, Yuan; Liu, Jun
  • Plant Biotechnology Journal, Vol. 11, Issue 5
  • DOI: 10.1111/pbi.12054

Constitutive expression of cell wall invertase genes increases grain yield and starch content in maize
journal, August 2013

  • Li, Bei; Liu, Hua; Zhang, Yue
  • Plant Biotechnology Journal, Vol. 11, Issue 9
  • DOI: 10.1111/pbi.12102

Silencing of vacuolar invertase and asparagine synthetase genes and its impact on acrylamide formation of fried potato products
journal, June 2015

  • Zhu, Xiaobiao; Gong, Huiling; He, Qunyan
  • Plant Biotechnology Journal, Vol. 14, Issue 2
  • DOI: 10.1111/pbi.12421

Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata
journal, January 2019

  • Wei, Tonglu; Wang, Yue; Xie, Zongzhou
  • Plant Biotechnology Journal, Vol. 17, Issue 7
  • DOI: 10.1111/pbi.13064

Cytosolic invertases contribute to cellulose biosynthesis and influence carbon partitioning in seedlings of Arabidopsis thaliana
journal, April 2018

  • Barnes, William J.; Anderson, Charles T.
  • The Plant Journal, Vol. 94, Issue 6
  • DOI: 10.1111/tpj.13909

The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006


Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling
journal, April 2014


SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006


Genetic Evidence for the Role of a Rice Vacuolar Invertase as a Molecular Sink Strength Determinant
journal, January 2018


The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato
journal, November 2017


Ectopic expression of a tobacco vacuolar invertase inhibitor in guard cells confers drought tolerance in Arabidopsis
journal, February 2016

  • Chen, Su-Fen; Liang, Ke; Yin, Dong-Mei
  • Journal of Enzyme Inhibition and Medicinal Chemistry, Vol. 31, Issue 6
  • DOI: 10.3109/14756366.2016.1142981

Regulation of assimilate import into sink organs: update on molecular drivers of sink strength
journal, January 2013

  • Bihmidine, Saadia; Hunter, Charles T.; Johns, Christine E.
  • Frontiers in Plant Science, Vol. 4
  • DOI: 10.3389/fpls.2013.00177

Sucrose and invertases, a part of the plant defense response to the biotic stresses
journal, June 2014


Targeting the AtCWIN1 Gene to Explore the Role of Invertases in Sucrose Transport in Roots and during Botrytis cinerea Infection
journal, December 2016

  • Veillet, Florian; Gaillard, Cécile; Coutos-Thévenot, Pierre
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.01899

Prolonged Expression of a Putative Invertase Inhibitor in Micropylar Endosperm Suppressed Embryo Growth in Arabidopsis
journal, January 2018


Genome-Wide Survey of Invertase Encoding Genes and Functional Characterization of an Extracellular Fungal Pathogen-Responsive Invertase in Glycine max
journal, August 2018

  • Su, Tao; Han, Mei; Min, Jie
  • International Journal of Molecular Sciences, Vol. 19, Issue 8
  • DOI: 10.3390/ijms19082395

A 6&1-FEH Encodes an Enzyme for Fructan Degradation and Interact with Invertase Inhibitor Protein in Maize (Zea mays L.)
journal, August 2019

  • Zhao, Hongbo; Greiner, Steffen; Scheffzek, Klaus
  • International Journal of Molecular Sciences, Vol. 20, Issue 15
  • DOI: 10.3390/ijms20153807