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

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2019 Aug 7

PMID 31382684

Citations 4

Authors

Hongbo Zhao

Steffen Greiner

Klaus Scheffzek

Thomas Rausch

Guoping Wang

Affiliations

Soon will be listed here.

Abstract

About 15% of higher plants have acquired the ability to convert sucrose into fructans. Fructan degradation is catalyzed by fructan exohydrolases (FEHs), which are structurally related to cell wall invertases (CWI). However, the biological function(s) of FEH enzymes in non-fructan species have remained largely enigmatic. In the present study, one maize CWI-related enzyme named Zm-6&1-FEH1, displaying FEH activity, was explored with respect to its substrate specificities, its expression during plant development, and its possible interaction with CWI inhibitor protein. Following heterologous expression in and in leaves, recombinant Zm-6&1-FEH1 revealed substrate specificities of levan and inulin, and also displayed partially invertase activity. Expression of Zm-6&1-FEH1 as monitored by qPCR was strongly dependent on plant development and was further modulated by abiotic stress. To explore whether maize FEH can interact with invertase inhibitor protein, Zm-6&1-FEH1 and maize invertase inhibitor Zm-INVINH1 were co-expressed in leaves. Bimolecular fluorescence complementation (BiFC) analysis and in vitro enzyme inhibition assays indicated productive complex formation. In summary, the results provide support to the hypothesis that in non-fructan species FEH enzymes may modulate the regulation of CWIs.

Citing Articles

Evidence for Light and Tissue Specific Regulation of Genes Involved in Fructan Metabolism in .

Gomez-Vargas A, Hernandez-Martinez K, Lopez-Rosas M, Alejo Jacuinde G, Simpson J Plants (Basel). 2022; 11(16).

PMID: 36015458 PMC: 9412663. DOI: 10.3390/plants11162153.

Functional Characterization of a Cucumber ( L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress.

Feng Z, Zheng F, Wu S, Li R, Li Y, Zhong J Int J Mol Sci. 2021; 22(17).

PMID: 34502273 PMC: 8431200. DOI: 10.3390/ijms22179365.

A Fructan Exohydrolase from Maize Degrades Both Inulin and Levan and Co-Exists with 1-Kestotriose in Maize.

Wu S, Greiner S, Ma C, Zhong J, Huang X, Rausch T Int J Mol Sci. 2021; 22(10).

PMID: 34068004 PMC: 8152283. DOI: 10.3390/ijms22105149.

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

Su T, Han M, Min J, Zhou H, Zhang Q, Zhao J Front Plant Sci. 2020; 10:1654.

PMID: 31969894 PMC: 6960229. DOI: 10.3389/fpls.2019.01654.

References

Scott A, Wyatt S, Tsou P, Robertson D, Allen N . Model system for plant cell biology: GFP imaging in living onion epidermal cells. Biotechniques. 1999; 26(6):1125, 1128-32. DOI: 10.2144/99266st04. View

Kim J, Mahe A, Guy S, Brangeon J, Roche O, Chourey P . Characterization of two members of the maize gene family, Incw3 and Incw4, encoding cell-wall invertases. Gene. 2000; 245(1):89-102. DOI: 10.1016/s0378-1119(00)00034-2. View

Hirose T, Takano M, Terao T . Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant Cell Physiol. 2002; 43(4):452-9. DOI: 10.1093/pcp/pcf055. View

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A . Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3(7):RESEARCH0034. PMC: 126239. DOI: 10.1186/gb-2002-3-7-research0034. View

Cheng W, Taliercio E, Chourey P . The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel. Plant Cell. 1996; 8(6):971-983. PMC: 161152. DOI: 10.1105/tpc.8.6.971. View

Van den Ende W, De Coninck B, Clerens S, Vergauwen R, Van Laere A . Unexpected presence of fructan 6-exohydrolases (6-FEHs) in non-fructan plants: characterization, cloning, mass mapping and functional analysis of a novel "cell-wall invertase-like" specific 6-FEH from sugar beet (Beta vulgaris L.). Plant J. 2003; 36(5):697-710. DOI: 10.1046/j.1365-313x.2003.01912.x. View

Bate N, Niu X, Wang Y, Reimann K, Helentjaris T . An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant Physiol. 2003; 134(1):246-54. PMC: 316304. DOI: 10.1104/pp.103.027466. View

Hothorn M, DAngelo I, Marquez J, Greiner S, Scheffzek K . The invertase inhibitor Nt-CIF from tobacco: a highly thermostable four-helix bundle with an unusual N-terminal extension. J Mol Biol. 2003; 335(4):987-95. DOI: 10.1016/j.jmb.2003.10.066. View

Rausch T, Greiner S . Plant protein inhibitors of invertases. Biochim Biophys Acta. 2004; 1696(2):253-61. DOI: 10.1016/j.bbapap.2003.09.017. View

10.

Pettersen E, Goddard T, Huang C, Couch G, Greenblatt D, Meng E . UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem. 2004; 25(13):1605-12. DOI: 10.1002/jcc.20084. View

11.

Link M, Rausch T, Greiner S . In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. FEBS Lett. 2004; 573(1-3):105-9. DOI: 10.1016/j.febslet.2004.07.062. View

12.

Verhaest M, Van den Ende W, Le Roy K, De Ranter C, Van Laere A, Rabijns A . X-ray diffraction structure of a plant glycosyl hydrolase family 32 protein: fructan 1-exohydrolase IIa of Cichorium intybus. Plant J. 2005; 41(3):400-11. DOI: 10.1111/j.1365-313X.2004.02304.x. View

13.

Chourey P, Jain M, Li Q, Carlson S . Genetic control of cell wall invertases in developing endosperm of maize. Planta. 2005; 223(2):159-67. DOI: 10.1007/s00425-005-0039-5. View

14.

Ji X, Van den Ende W, Schroeven L, Clerens S, Geuten K, Cheng S . The rice genome encodes two vacuolar invertases with fructan exohydrolase activity but lacks the related fructan biosynthesis genes of the Pooideae. New Phytol. 2006; 173(1):50-62. DOI: 10.1111/j.1469-8137.2006.01896.x. View

15.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

16.

Le Roy K, Verhaest M, Rabijns A, Clerens S, Van Laere A, Van den Ende W . N-glycosylation affects substrate specificity of chicory fructan 1-exohydrolase: evidence for the presence of an inulin binding cleft. New Phytol. 2007; 176(2):317-324. DOI: 10.1111/j.1469-8137.2007.02174.x. View

17.

Lammens W, Le Roy K, Van Laere A, Rabijns A, Van den Ende W . Crystal structures of Arabidopsis thaliana cell-wall invertase mutants in complex with sucrose. J Mol Biol. 2008; 377(2):378-85. DOI: 10.1016/j.jmb.2007.12.074. View

18.

Le Roy K, Lammens W, Van Laere A, Van den Ende W . Influencing the binding configuration of sucrose in the active sites of chicory fructan 1-exohydrolase and sugar beet fructan 6-exohydrolase. New Phytol. 2008; 178(3):572-80. DOI: 10.1111/j.1469-8137.2008.02386.x. View

19.

Alexandrov N, Brover V, Freidin S, Troukhan M, Tatarinova T, Zhang H . Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol. 2008; 69(1-2):179-94. PMC: 2709227. DOI: 10.1007/s11103-008-9415-4. View

20.

Kusch U, Harms K, Rausch T, Greiner S . Inhibitors of plant invertases do not affect the structurally related enzymes of fructan metabolism. New Phytol. 2008; 181(3):601-12. DOI: 10.1111/j.1469-8137.2008.02688.x. View