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 »
- Authors:
-
- 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:
Post-Translational Derepression of Invertase Activity in Source Leaves via Down-Regulation of Invertase Inhibitor Expression Is Part of the Plant Defense Response
journal, November 2010
- Bonfig, Katharina B.; Gabler, Andrea; Simon, Uwe K.
- Molecular Plant, Vol. 3, Issue 6
RNA Interference of LIN5 in Tomato Confirms Its Role in Controlling Brix Content, Uncovers the Influence of Sugars on the Levels of Fruit Hormones, and Demonstrates the Importance of Sucrose Cleavage for Normal Fruit Development and Fertility
journal, May 2009
- Zanor, María Inés; Osorio, Sonia; Nunes-Nesi, Adriano
- Plant Physiology, Vol. 150, Issue 3
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
Molecular cloning, expression and characterization of a novel apoplastic invertase inhibitor from tomato (Solanum lycopersicum) and its use to purify a vacuolar invertase
journal, November 2008
- Reca, Ida Barbara; Brutus, Alexandre; D'Avino, Rossana
- Biochimie, Vol. 90, Issue 11-12
Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development
journal, June 2004
- Koch, Karen
- Current Opinion in Plant Biology, Vol. 7, Issue 3
Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean ( Glycine max )
journal, December 2016
- Tang, Xiaofei; Su, Tao; Han, Mei
- Journal of Experimental Botany
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
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
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
Genetic Evidence for the Role of a Rice Vacuolar Invertase as a Molecular Sink Strength Determinant
journal, January 2018
- Morey, Shamitha Rao; Hirose, Tatsuro; Hashida, Yoichi
- Rice, Vol. 11, Issue 1
The riddle of mitochondrial alkaline/neutral invertases: A novel Arabidopsis isoform mainly present in reproductive tissues and involved in root ROS production
journal, September 2017
- Battaglia, Marina E.; Martin, María Victoria; Lechner, Leandra
- PLOS ONE, Vol. 12, Issue 9
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
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
Posttranslational Elevation of Cell Wall Invertase Activity by Silencing Its Inhibitor in Tomato Delays Leaf Senescence and Increases Seed Weight and Fruit Hexose Level
journal, July 2009
- Jin, Ye; Ni, Di-An; Ruan, Yong-Ling
- The Plant Cell, Vol. 21, Issue 7
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
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
Tolerance to drought and salt stress in plants: Unraveling the signaling networks
journal, April 2014
- Golldack, Dortje; Li, Chao; Mohan, Harikrishnan
- Frontiers in Plant Science, Vol. 5
Reassessment of an Arabidopsis cell wall invertase inhibitor AtCIF1 reveals its role in seed germination and early seedling growth
journal, November 2015
- Su, Tao; Wolf, Sebastian; Han, Mei
- Plant Molecular Biology, Vol. 90, Issue 1-2
Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew
journal, June 2006
- Swarbrick, Philip J.; Schulze-Lefert, Paul; Scholes, Julie D.
- Plant, Cell and Environment, Vol. 29, Issue 6
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
Populus : A Model System for Plant Biology
journal, June 2007
- Jansson, Stefan; Douglas, Carl J.
- Annual Review of Plant Biology, Vol. 58, Issue 1
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
Enzyme Inhibitor Studies Reveal Complex Control of Methyl-D-Erythritol 4-Phosphate (MEP) Pathway Enzyme Expression in Catharanthus roseus
journal, May 2013
- Han, Mei; Heppel, Simon C.; Su, Tao
- PLoS ONE, Vol. 8, Issue 5
Evolution and diversity of invertase genes in Populus trichocarpa
journal, October 2007
- Bocock, Philip N.; Morse, Alison M.; Dervinis, Christopher
- Planta, Vol. 227, Issue 3
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
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
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
Plant–Pathogen Maneuvering over Apoplastic Sugars
journal, September 2017
- Naseem, Muhammad; Kunz, Meik; Dandekar, Thomas
- Trends in Plant Science, Vol. 22, Issue 9
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
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
GSDS 2.0: an upgraded gene feature visualization server
journal, December 2014
- Hu, Bo; Jin, Jinpu; Guo, An-Yuan
- Bioinformatics, Vol. 31, Issue 8
Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond
journal, February 2018
- Wan, Hongjian; Wu, Limin; Yang, Yuejian
- Trends in Plant Science, Vol. 23, Issue 2
Cell Wall-Bound Invertase Limits Sucrose Export and Is Involved in Symptom Development and Inhibition of Photosynthesis during Compatible Interaction between Tomato and Xanthomonas campestris pv vesicatoria
journal, September 2008
- Kocal, Nurcan; Sonnewald, Uwe; Sonnewald, Sophia
- Plant Physiology, Vol. 148, Issue 3
New Insights into Roles of Cell Wall Invertase in Early Seed Development Revealed by Comprehensive Spatial and Temporal Expression Patterns of GhCWIN1 in Cotton
journal, August 2012
- Wang, Lu; Ruan, Yong-Ling
- Plant Physiology, Vol. 160, Issue 2
Plant protein inhibitors of invertases
journal, February 2004
- Rausch, Thomas; Greiner, Steffen
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1696, Issue 2
Simple, rapid and efficient transformation of genotype Nisqually-1: a basic tool for the first sequenced model tree
journal, June 2017
- Li, Shujuan; Zhen, Cheng; Xu, Wenjing
- Scientific Reports, Vol. 7, Issue 1
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
An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth
journal, April 2006
- Kohorn, Bruce D.; Kobayashi, Masaru; Johansen, Sue
- The Plant Journal, Vol. 46, Issue 2
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
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
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
Tomato Ovary-to-Fruit Transition is Characterized by a Spatial Shift of mRNAs for Cell Wall Invertase and its Inhibitor with the Encoded Proteins Localized to Sieve Elements
journal, February 2015
- Palmer, William M.; Ru, Lei; Jin, Ye
- Molecular Plant, Vol. 8, Issue 2
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
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
In Arabidopsis thaliana , the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles
journal, August 2004
- Link, Manuela; Rausch, Thomas; Greiner, Steffen
- FEBS Letters, Vol. 573, Issue 1-3
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
Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat: Reproductive stage drought tolerance in wheat
journal, March 2010
- Ji, Xuemei; Shiran, Behrouz; Wan, Jianlin
- Plant, Cell & Environment, Vol. 33, Issue 6
Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana: Invertase and clubroot disease
journal, October 2010
- Siemens, Johannes; GonzÁLez, Maria-Cruz; Wolf, Sebastian
- Molecular Plant Pathology, Vol. 12, Issue 3
Sucrose and invertases, a part of the plant defense response to the biotic stresses
journal, June 2014
- Tauzin, Alexandra S.; Giardina, Thierry
- Frontiers in Plant Science, Vol. 5
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
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
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
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
Genetic control of cell wall invertases in developing endosperm of maize
journal, July 2005
- Chourey, Prem S.; Jain, Mukesh; Li, Qin-Bao
- Planta, Vol. 223, Issue 2
Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes: Donor and acceptor substrate selectivity in GH32
journal, September 2009
- Van den Ende, Wim; Lammens, Willem; Van Laere, André
- FEBS Journal, Vol. 276, Issue 20
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
Sugar transporters in plants and in their interactions with fungi
journal, July 2012
- Doidy, Joan; Grace, Emily; Kühn, Christina
- Trends in Plant Science, Vol. 17, Issue 7
Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice: Cell wall invertase modulates disease resistance
journal, October 2013
- Sun, Li; Yang, Dong-lei; Kong, Yu
- Molecular Plant Pathology, Vol. 15, Issue 2
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
journal, June 2002
- Vandesompele, Jo; De Preter, Katleen; Pattyn, Filip
- Genome Biology, Vol. 3, Issue 7
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006
- Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen
- Annual Review of Plant Biology, Vol. 57, Issue 1
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
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
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
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
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
Antisense Acid Invertase (TIV1) Gene Alters Soluble Sugar Composition and Size in Transgenic Tomato Fruit
journal, November 1996
- Klann, E. M.; Hall, B.; Bennett, A. B.
- Plant Physiology, Vol. 112, Issue 3
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
Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling
journal, April 2014
- Ruan, Yong-Ling
- Annual Review of Plant Biology, Vol. 65, Issue 1
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
Prolonged Expression of a Putative Invertase Inhibitor in Micropylar Endosperm Suppressed Embryo Growth in Arabidopsis
journal, January 2018
- Zuma, Bongeka; Dana, Mason B.; Wang, Dongfang
- Frontiers in Plant Science, Vol. 9
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
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
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
HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree)
journal, January 2015
- Liu, Shujin; Lan, Jixian; Zhou, Binhui
- New Phytologist, Vol. 206, Issue 2
Genome-Wide Characterization of AspATs in Populus: Gene Expression Variation and Enzyme Activities in Response to Nitrogen Perturbations
journal, May 2019
- Su, Tao; Han, Mei; Min, Jie
- Forests, Vol. 10, Issue 5
Aberrant seed development in Litchi chinensis is associated with the impaired expression of cell wall invertase genes
journal, August 2018
- Zhang, Jieqiong; Wu, Zichen; Hu, Fuchu
- Horticulture Research, Vol. 5, Issue 1
Invertases. Primary Structures, Functions, and Roles in Plant Development and Sucrose Partitioning
journal, September 1999
- Sturm, Arnd
- Plant Physiology, Vol. 121, Issue 1
Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers: Invertase inhibitor affects cold sweetening
journal, July 2012
- Mckenzie, Marian J.; Chen, Ronan K. Y.; Harris, John C.
- Plant, Cell & Environment, Vol. 36, Issue 1
Mathematical Modeling of the Central Carbohydrate Metabolism in Arabidopsis Reveals a Substantial Regulatory Influence of Vacuolar Invertase on Whole Plant Carbon Metabolism
journal, March 2010
- Nägele, Thomas; Henkel, Sebastian; Hörmiller, Imke
- Plant Physiology, Vol. 153, Issue 1
The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato
journal, November 2017
- Xu, Xiao-xia; Hu, Qin; Yang, Wan-nian
- BMC Plant Biology, Vol. 17, Issue 1
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
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
CsINV5, a tea vacuolar invertase gene enhances cold tolerance in transgenic Arabidopsis
journal, October 2018
- Qian, Wenjun; Xiao, Bin; Wang, Lu
- BMC Plant Biology, Vol. 18, Issue 1
Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins
journal, March 1997
- Ehness, Rainer; Roitsch, Thomas
- The Plant Journal, Vol. 11, Issue 3
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
Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis
journal, November 2003
- Wolf, Sebastian; Grsic-Rausch, Slobodanka; Rausch, Thomas
- FEBS Letters, Vol. 555, Issue 3
An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020
- Dong, Wentao; Zhu, Yayun; Chang, Huizhong
- Nature, Vol. 589, Issue 7843
Ectopic expression of a tobacco vacuolar invertase inhibitor in guard cells confers drought tolerance in Arabidopsis
text, January 2016
- Chen, Su-Fen; Liang, Ke; Yin, Dong-Mei
- Taylor & Francis
Ectopic expression of a tobacco vacuolar invertase inhibitor in guard cells confers drought tolerance in Arabidopsis
text, January 2016
- Chen, Su-Fen; Liang, Ke; Yin, Dong-Mei
- Taylor & Francis
Genetic control of cell wall invertases in developing endosperm of maize
journal, July 2005
- Chourey, Prem S.; Jain, Mukesh; Li, Qin-Bao
- Planta, Vol. 223, Issue 2
Molecular cloning, expression and characterization of a novel apoplastic invertase inhibitor from tomato (Solanum lycopersicum) and its use to purify a vacuolar invertase
journal, November 2008
- Reca, Ida Barbara; Brutus, Alexandre; D'Avino, Rossana
- Biochimie, Vol. 90, Issue 11-12
In Arabidopsis thaliana , the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles
journal, August 2004
- Link, Manuela; Rausch, Thomas; Greiner, Steffen
- FEBS Letters, Vol. 573, Issue 1-3
Tomato Ovary-to-Fruit Transition is Characterized by a Spatial Shift of mRNAs for Cell Wall Invertase and its Inhibitor with the Encoded Proteins Localized to Sieve Elements
journal, February 2015
- Palmer, William M.; Ru, Lei; Jin, Ye
- Molecular Plant, Vol. 8, Issue 2
Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development
journal, June 2004
- Koch, Karen
- Current Opinion in Plant Biology, Vol. 7, Issue 3
Sugar transporters in plants and in their interactions with fungi
journal, July 2012
- Doidy, Joan; Grace, Emily; Kühn, Christina
- Trends in Plant Science, Vol. 17, Issue 7
Plant–Pathogen Maneuvering over Apoplastic Sugars
journal, September 2017
- Naseem, Muhammad; Kunz, Meik; Dandekar, Thomas
- Trends in Plant Science, Vol. 22, Issue 9
Evolution of Sucrose Metabolism: The Dichotomy of Invertases and Beyond
journal, February 2018
- Wan, Hongjian; Wu, Limin; Yang, Yuejian
- Trends in Plant Science, Vol. 23, Issue 2
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
Aberrant seed development in Litchi chinensis is associated with the impaired expression of cell wall invertase genes
journal, August 2018
- Zhang, Jieqiong; Wu, Zichen; Hu, Fuchu
- Horticulture Research, Vol. 5, Issue 1
Influence of cluster thinning and girdling on aroma composition in ‘Jumeigui’ table grape
journal, April 2020
- Xi, Xiaojun; Zha, Qian; He, Yani
- Scientific Reports, Vol. 10, Issue 1
Characterization and phylogenetic analysis of the complete mitochondrial genome of the pathogenic fungus Ilyonectria destructans
journal, February 2022
- Androsiuk, Piotr; Okorski, Adam; Paukszto, Łukasz
- Scientific Reports, Vol. 12, Issue 1
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
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
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
GSDS 2.0: an upgraded gene feature visualization server
journal, December 2014
- Hu, Bo; Jin, Jinpu; Guo, An-Yuan
- Bioinformatics, Vol. 31, Issue 8
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
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
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
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
Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean ( Glycine max )
journal, December 2016
- Tang, Xiaofei; Su, Tao; Han, Mei
- Journal of Experimental Botany
Post-Translational Derepression of Invertase Activity in Source Leaves via Down-Regulation of Invertase Inhibitor Expression Is Part of the Plant Defense Response
journal, November 2010
- Bonfig, Katharina B.; Gabler, Andrea; Simon, Uwe K.
- Molecular Plant, Vol. 3, Issue 6
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
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
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
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
RNA Interference of LIN5 in Tomato Confirms Its Role in Controlling Brix Content, Uncovers the Influence of Sugars on the Levels of Fruit Hormones, and Demonstrates the Importance of Sucrose Cleavage for Normal Fruit Development and Fertility
journal, May 2009
- Zanor, María Inés; Osorio, Sonia; Nunes-Nesi, Adriano
- Plant Physiology, Vol. 150, Issue 3
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
Antisense Acid Invertase (TIV1) Gene Alters Soluble Sugar Composition and Size in Transgenic Tomato Fruit
journal, November 1996
- Klann, E. M.; Hall, B.; Bennett, A. B.
- Plant Physiology, Vol. 112, Issue 3
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
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
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
Posttranslational Elevation of Cell Wall Invertase Activity by Silencing Its Inhibitor in Tomato Delays Leaf Senescence and Increases Seed Weight and Fruit Hexose Level
journal, July 2009
- Jin, Ye; Ni, Di-An; Ruan, Yong-Ling
- The Plant Cell, Vol. 21, Issue 7
Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew
journal, June 2006
- Swarbrick, Philip J.; Schulze-Lefert, Paul; Scholes, Julie D.
- Plant, Cell and Environment, Vol. 29, Issue 6
An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth
journal, April 2006
- Kohorn, Bruce D.; Kobayashi, Masaru; Johansen, Sue
- The Plant Journal, Vol. 46, Issue 2
Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes: Donor and acceptor substrate selectivity in GH32
journal, September 2009
- Van den Ende, Wim; Lammens, Willem; Van Laere, André
- FEBS Journal, Vol. 276, Issue 20
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
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
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
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
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
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
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
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Sucrose Metabolism: Gateway to Diverse Carbon Use and Sugar Signaling
journal, April 2014
- Ruan, Yong-Ling
- Annual Review of Plant Biology, Vol. 65, Issue 1
SUGAR SENSING AND SIGNALING IN PLANTS: Conserved and Novel Mechanisms
journal, June 2006
- Rolland, Filip; Baena-Gonzalez, Elena; Sheen, Jen
- Annual Review of Plant Biology, Vol. 57, Issue 1
Genetic Evidence for the Role of a Rice Vacuolar Invertase as a Molecular Sink Strength Determinant
journal, January 2018
- Morey, Shamitha Rao; Hirose, Tatsuro; Hashida, Yoichi
- Rice, Vol. 11, Issue 1
The roles of cell wall invertase inhibitor in regulating chilling tolerance in tomato
journal, November 2017
- Xu, Xiao-xia; Hu, Qin; Yang, Wan-nian
- BMC Plant Biology, Vol. 17, Issue 1
Enzyme Inhibitor Studies Reveal Complex Control of Methyl-D-Erythritol 4-Phosphate (MEP) Pathway Enzyme Expression in Catharanthus roseus
journal, May 2013
- Han, Mei; Heppel, Simon C.; Su, Tao
- PLoS ONE, Vol. 8, Issue 5
The riddle of mitochondrial alkaline/neutral invertases: A novel Arabidopsis isoform mainly present in reproductive tissues and involved in root ROS production
journal, September 2017
- Battaglia, Marina E.; Martin, María Victoria; Lechner, Leandra
- PLOS ONE, Vol. 12, Issue 9
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
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
Sucrose and invertases, a part of the plant defense response to the biotic stresses
journal, June 2014
- Tauzin, Alexandra S.; Giardina, Thierry
- Frontiers in Plant Science, Vol. 5
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
Prolonged Expression of a Putative Invertase Inhibitor in Micropylar Endosperm Suppressed Embryo Growth in Arabidopsis
journal, January 2018
- Zuma, Bongeka; Dana, Mason B.; Wang, Dongfang
- Frontiers in Plant Science, Vol. 9
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
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