HvBGlu3, a GH1 β-glucosidase Enzyme Gene, Negatively Influences β-glucan Content in Barley Grains

Overview

Journal Theor Appl Genet

Publisher Springer

Specialty Genetics

Date 2024 Jan 2

PMID 38165440

Authors

La Geng

Mengdi Li

Shanggeng Xie

Han Wang

Xinyi He

Nannan Sun

Guoping Zhang

Lingzhen Ye

Affiliations

Soon will be listed here.

Abstract

HvBGlu3, a β-glucosidase enzyme gene, negatively influences β-glucan content in barley grains by mediating starch and sucrose metabolism in developing grains. Barley grains are rich in β-glucan, an important factor affecting end-use quality. Previously, we identified several stable marker-trait associations (MTAs) and novel candidate genes associated with β-glucan content in barley grains using GWAS (Genome Wide Association Study) analysis. The gene HORVU3Hr1G096910, encoding β-glucosidase 3, named HvBGlu3, is found to be associated with β-glucan content in barley grains. In this study, conserved domain analysis suggested that HvBGlu3 belongs to glycoside hydrolase family 1 (GH1). Gene knockout assay revealed that HvBGlu3 negatively influenced β-glucan content in barley grains. Transcriptome analysis of developing grains of hvbglu3 mutant and the wild type indicated that the knockout of the gene led to the increased expression level of genes involved in starch and sucrose metabolism. Glucose metabolism analysis showed that the contents of many sugars in developing grains were significantly changed in hvbglu3 mutants. In conclusion, HvBGlu3 modulates β-glucan content in barley grains by mediating starch and sucrose metabolism in developing grains. The obtained results may be useful for breeders to breed elite barley cultivars for food use by screening barley lines with loss of function of HvBGlu3 in barley breeding.

References

Brunner F, Wirtz W, Rose J, Darvill A, Govers F, Scheel D . A beta-glucosidase/xylosidase from the phytopathogenic oomycete, Phytophthora infestans. Phytochemistry. 2002; 59(7):689-96. DOI: 10.1016/s0031-9422(02)00045-6. View

Burton R, Wilson S, Hrmova M, Harvey A, Shirley N, Medhurst A . Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-beta-D-glucans. Science. 2006; 311(5769):1940-2. DOI: 10.1126/science.1122975. View

Burton R, Gidley M, Fincher G . Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol. 2010; 6(10):724-32. DOI: 10.1038/nchembio.439. View

Burton R, Collins H, Kibble N, Smith J, Shirley N, Jobling S . Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure. Plant Biotechnol J. 2010; 9(2):117-35. DOI: 10.1111/j.1467-7652.2010.00532.x. View

Cantarel B, Coutinho P, Rancurel C, Bernard T, Lombard V, Henrissat B . The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2008; 37(Database issue):D233-8. PMC: 2686590. DOI: 10.1093/nar/gkn663. View

Clarke B, Liang R, Morell M, Bird A, Jenkins C, Li Z . Gene expression in a starch synthase IIa mutant of barley: changes in the level of gene transcription and grain composition. Funct Integr Genomics. 2008; 8(3):211-21. DOI: 10.1007/s10142-007-0070-7. View

Feng X, Liu W, Qiu C, Zeng F, Wang Y, Zhang G . HvAKT2 and HvHAK1 confer drought tolerance in barley through enhanced leaf mesophyll H homoeostasis. Plant Biotechnol J. 2020; 18(8):1683-1696. PMC: 7336388. DOI: 10.1111/pbi.13332. View

Fincher G . Exploring the evolution of (1,3;1,4)-beta-D-glucans in plant cell walls: comparative genomics can help!. Curr Opin Plant Biol. 2009; 12(2):140-7. DOI: 10.1016/j.pbi.2009.01.002. View

Garcia-Gimenez G, Russell J, Aubert M, Fincher G, Burton R, Waugh R . Barley grain (1,3;1,4)-β-glucan content: effects of transcript and sequence variation in genes encoding the corresponding synthase and endohydrolase enzymes. Sci Rep. 2019; 9(1):17250. PMC: 6872655. DOI: 10.1038/s41598-019-53798-8. View

10.

Garcia-Gimenez G, Barakate A, Smith P, Stephens J, Khor S, Doblin M . Targeted mutation of barley (1,3;1,4)-β-glucan synthases reveals complex relationships between the storage and cell wall polysaccharide content. Plant J. 2020; 104(4):1009-1022. DOI: 10.1111/tpj.14977. View

11.

Guillon F, Bouchet B, Jamme F, Robert P, Quemener B, Barron C . Brachypodium distachyon grain: characterization of endosperm cell walls. J Exp Bot. 2010; 62(3):1001-15. DOI: 10.1093/jxb/erq332. View

12.

Han F, Ullrich S, Chirat S, Menteur S, Jestin L, Sarrafi A . Mapping of β-glucan content and β-glucanase activity loci in barley grain and malt. Theor Appl Genet. 2013; 91(6-7):921-7. DOI: 10.1007/BF00223901. View

13.

Henrissat B . A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 1991; 280 ( Pt 2):309-16. PMC: 1130547. DOI: 10.1042/bj2800309. View

14.

Hill A, Reilly P . Computational analysis of glycoside hydrolase family 1 specificities. Biopolymers. 2008; 89(11):1021-31. DOI: 10.1002/bip.21052. View

15.

Hrmova M, Harvey A, Wang J, Shirley N, Jones G, Stone B . Barley beta-D-glucan exohydrolases with beta-D-glucosidase activity. Purification, characterization, and determination of primary structure from a cDNA clone. J Biol Chem. 1996; 271(9):5277-86. DOI: 10.1074/jbc.271.9.5277. View

16.

Hrmova M, Burton R, Biely P, Lahnstein J, Fincher G . Hydrolysis of (1,4)-beta-D-mannans in barley (Hordeum vulgare L.) is mediated by the concerted action of (1,4)-beta-D-mannan endohydrolase and beta-D-mannosidase. Biochem J. 2006; 399(1):77-90. PMC: 1570163. DOI: 10.1042/BJ20060170. View

17.

Hughes J, Grafenauer S . Oat and Barley in the Food Supply and Use of Beta Glucan Health Claims. Nutrients. 2021; 13(8). PMC: 8401220. DOI: 10.3390/nu13082556. View

18.

Izydorczyk M, Storsley J, Labossiere D, Macgregor A, Rossnagel B . Variation in total and soluble beta-glucan content in hulless barley: effects of thermal, physical, and enzymic treatments. J Agric Food Chem. 2000; 48(4):982-9. DOI: 10.1021/jf991102f. View

19.

Jacob J, Pescatore A . Barley β-glucan in poultry diets. Ann Transl Med. 2014; 2(2):20. PMC: 4202475. DOI: 10.3978/j.issn.2305-5839.2014.01.02. View

20.

Kim D, Paggi J, Park C, Bennett C, Salzberg S . Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37(8):907-915. PMC: 7605509. DOI: 10.1038/s41587-019-0201-4. View