A novel polymorphism in the 5′ UTR of HvDEP1 is associated with grain length and 1000-grain weight in barley (Hordeum vulgare)
Calum Watt
A B E , Gaofeng Zhou A B , Tefera Tolera Angessa A B , David Moody C and Chengdao Li A B D E
+ Author Affiliations
- Author Affiliations
A Western Crop Genetics Alliance, Murdoch University, 90 South Street, WA 6150, Australia.
B Western Australian State Agricultural Biotechnology Centre, Murdoch University, 90 South Street,WA 6150, Australia.
C Intergrain Pty Ltd, 19 Ambitious Link, Bibra Lake, WA 6163, Australia.
D Department of Primary Industries and Regional Development, WA, Australia.
E Corresponding authors. Email: C.li@murdoch.edu.au; calumwatt12@outlook.com
Crop and Pasture Science 71(8) 752-759 https://doi.org/10.1071/CP20169
Submitted: 22 May 2020 Accepted: 5 August 2020 Published: 18 August 2020
Journal Compilation © CSIRO 2020 Open Access CC BY-NC-ND
Abstract
The gene HvDEP1, on barley (Hordeum vulgare L.) chromosome 5H, encodes a γ-subunit of the heterotrimeric G-protein complex and was previously determined to be a candidate gene underlying a major quantitative trait locus for grain length. In the present study, we identified a 9 bp indel (insertion–deletion mutation) at position –84 bp from the start codon within a reported upstream open reading frame located in the 5′ UTR (untranslated region) and developed a diagnostic molecular marker. We also identified a 13 bp indel (–514 bp) in linkage disequilibrium that bridges an important regulatory motif. Using a doubled-haploid population and a barley diversity panel, we were able to show that the effects of these indels were environmentally stable and consistently delineated phenotypic groups based on grain length and 1000-grain weight. Genotypes represented by deletions at these two positions relative to the reference cv. Morex had consistently shorter grains, by 3.69–3.96%, and lower 1000-grain weight, by 2.38–4.21%, in a doubled-haploid population studied. Additionally, a diversity panel was tested but consistent differences were observed only for grain length, reinforcing literature indicating the importance of this gene for grain-length regulation. The frequency of the longer and heavier grained reference allele was higher in modern cultivars, suggesting that indirect selection for longer grain may have occurred through direct selection for grain yield via grain-weight improvement. These results indicate that grain length and 1000-grain weight in barley can be manipulated by targeting variation in gene promoters through marker-assisted selection.
Additional keywords: cis-element, DEP1, grain length, promoter, TGW, uORF.
References
Ahmed I, Islam M, Arshad W, Mannan A, Ahmad W, Mirza B (2009) High-quality plant DNA extraction for PCR: an easy approach. Journal of Applied Genetics 50, 105–107.| High-quality plant DNA extraction for PCR: an easy approach.Crossref | GoogleScholarGoogle Scholar | 19433907PubMed |
Avni R, Oren L, Shabtay G, Assili S, Pozniak C, Hale I, Ben-David R, Peleg Z, Distelfeld A (2018) Genome based meta-QTL analysis of grain weight in tetraploid wheat identifies rare alleles of GRF4 associated with larger grains. Genes 9, 636
| Genome based meta-QTL analysis of grain weight in tetraploid wheat identifies rare alleles of GRF4 associated with larger grains.Crossref | GoogleScholarGoogle Scholar |
Bélanger S, Gauthier M, Jean M, Sato K, Belzile F (2014) Genomic characterization of the Hordeum vulgare DEP1 (HvDEP1) gene and its diversity in a collection of barley accessions. Euphytica 198, 29–41.
| Genomic characterization of the Hordeum vulgare DEP1 (HvDEP1) gene and its diversity in a collection of barley accessions.Crossref | GoogleScholarGoogle Scholar |
Colmsee C, Beier S, Himmelbach A, Schmutzer T, Stein N, Scholz U, Mascher M (2015) BARLEX: the barley draft genome explorer. Molecular Plant 8, 964–966.
| BARLEX: the barley draft genome explorer.Crossref | GoogleScholarGoogle Scholar | 25804976PubMed |
Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X (2009) Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics 41, 494–497.
| Natural variation at the DEP1 locus enhances grain yield in rice.Crossref | GoogleScholarGoogle Scholar | 19305410PubMed |
Jorgensen R, Dorantes-Acosta A (2012) Conserved peptide upstream open reading frames are associated with regulatory genes in angiosperms. Frontiers in Plant Science 3, 191
| Conserved peptide upstream open reading frames are associated with regulatory genes in angiosperms.Crossref | GoogleScholarGoogle Scholar | 22936940PubMed |
Karamyshev AL, Karamysheva ZN (2018) Lost in translation: ribosome-associated mRNA and protein quality controls. Frontiers in Genetics 9, 431
| Lost in translation: ribosome-associated mRNA and protein quality controls.Crossref | GoogleScholarGoogle Scholar | 30337940PubMed |
Ku L, Wei X, Zhang S, Zhang J, Guo S, Chen Y (2011) Cloning and characterization of a putative TAC1 ortholog associated with leaf angle in maize (Zea mays L.). PLoS One 6, e20621
| Cloning and characterization of a putative TAC1 ortholog associated with leaf angle in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 21687735PubMed |
Laing WA, Martínez-Sánchez M, Wright MA, Bulley SM, Brewster D, Dare AP, Rassam M, Wang D, Storey R, Macknight RC, Hellens RP (2015) An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in Arabidopsis. The Plant Cell 27, 772–786.
| An upstream open reading frame is essential for feedback regulation of ascorbate biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25724639PubMed |
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325–327.
| PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences.Crossref | GoogleScholarGoogle Scholar | 11752327PubMed |
Li X, Tao Q, Miao J, Yang Z, Gu M, Liang G, Zhou Y (2019) Evaluation of differential qPE9-1/DEP1 protein domains in rice grain length and weight variation. Rice 12, 5–15.
| Evaluation of differential qPE9-1/DEP1 protein domains in rice grain length and weight variation.Crossref | GoogleScholarGoogle Scholar | 30706248PubMed |
Liu L, Xu W, Hu X, Liu H, Lin Y (2016) W-box and G-box elements play important roles in early senescence of rice flag leaf. Scientific Reports 6, 20881
| W-box and G-box elements play important roles in early senescence of rice flag leaf.Crossref | GoogleScholarGoogle Scholar | 26864250PubMed |
Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, et al. (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544, 427–433.
| A chromosome conformation capture ordered sequence of the barley genome.Crossref | GoogleScholarGoogle Scholar | 28447635PubMed |
Mayer KFX, Waugh R, Langridge P, Close TJ, Wise RP, Graner A, Matsumoto T, Sato K, Schulman A, Muehlbauer GJ, et al. (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491, 711–716.
| A physical, genetic and functional sequence assembly of the barley genome.Crossref | GoogleScholarGoogle Scholar |
Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends in Biochemical Sciences 20, 506–510.
| The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins.Crossref | GoogleScholarGoogle Scholar | 8571452PubMed |
Morris DR, Geballe AP (2000) Upstream open reading frames as regulators of mRNA translation. Molecular and Cellular Biology 20, 8635–8642.
| Upstream open reading frames as regulators of mRNA translation.Crossref | GoogleScholarGoogle Scholar | 11073965PubMed |
Ramegowda V, Gill US, Sivalingam PN, Gupta A, Gupta C, Govind G, Nataraja KN, Pereira A, Udayakumar M, Mysore KS, Senthil-Kumar M (2017) GBF3 transcription factor imparts drought tolerance in Arabidopsis thaliana. Scientific Reports 7, 9148
| GBF3 transcription factor imparts drought tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 28831141PubMed |
Ravel C, Fiquet S, Boudet J, Dardevet M, Vincent J, Merlino M, Michard R, Martre P (2014) Conserved cis-regulatory modules in promoters of genes encoding wheat high-molecular-weight glutenin subunits. Frontiers in Plant Science 5, 1–17.
| Conserved cis-regulatory modules in promoters of genes encoding wheat high-molecular-weight glutenin subunits.Crossref | GoogleScholarGoogle Scholar |
Roy SC, Shil P (2020) Assessment of genetic heritability in rice breeding lines based on morphological traits and caryopsis ultrastructure. Scientific Reports 10, 7830
| Assessment of genetic heritability in rice breeding lines based on morphological traits and caryopsis ultrastructure.Crossref | GoogleScholarGoogle Scholar | 32385288PubMed |
Schnaithmann F, Pillen K (2013) Detection of exotic QTLs controlling nitrogen stress tolerance among wild barley introgression lines. Euphytica 189, 67–88.
| Detection of exotic QTLs controlling nitrogen stress tolerance among wild barley introgression lines.Crossref | GoogleScholarGoogle Scholar |
Shoemaker CJ, Green R (2012) Translation drives mRNA quality control. Nature Structural & Molecular Biology 19, 594–601.
| Translation drives mRNA quality control.Crossref | GoogleScholarGoogle Scholar |
Song XJ, Kuroha T, Ayano M, Furuta T, Nagai K, Komeda N, Segami S, Miura K, Ogawa D, Kamura T, et al. (2015) Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice. Proceedings of the National Academy of Sciences of the United States of America 112, 76–81.
| Rare allele of a previously unidentified histone H4 acetyltransferase enhances grain weight, yield, and plant biomass in rice.Crossref | GoogleScholarGoogle Scholar | 25535376PubMed |
Srivastava AK, Lu Y, Zinta G, Lang Z, Zhu J-K (2018) UTR-dependent control of gene expression in plants. Trends in Plant Science 23, 248–259.
| UTR-dependent control of gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 29223924PubMed |
Sun S, Wang L, Mao H, Shao L, Li X, Xiao J, Ouyang Y, Zhang Q (2018) A G-protein pathway determines grain size in rice. Nature Communications 9, 851
| A G-protein pathway determines grain size in rice.Crossref | GoogleScholarGoogle Scholar | 29487318PubMed |
Wan XY, Wan JM, Jiang L, Wang JK, Zhai HQ, Weng JF, Wang HL, Lei CL, Wang JL, Zhang X, Cheng ZJ, Guo XP (2006) QTL analysis for rice grain length and fine mapping of an identified QTL with stable and major effects. Theoretical and Applied Genetics 112, 1258–1270.
| QTL analysis for rice grain length and fine mapping of an identified QTL with stable and major effects.Crossref | GoogleScholarGoogle Scholar | 16477428PubMed |
Wang W, Simmonds J, Pan Q, Davidson D, He F, Battal A, Akhunova A, Trick HN, Uauy C, Akhunov E (2018) Gene editing and mutagenesis reveal inter-cultivar differences and additivity in the contribution of TaGW2 homoeologues to grain size and weight in wheat. Theoretical and Applied Genetics 131, 2463–2475.
| Gene editing and mutagenesis reveal inter-cultivar differences and additivity in the contribution of TaGW2 homoeologues to grain size and weight in wheat.Crossref | GoogleScholarGoogle Scholar | 30136108PubMed |
Watt C, Zhou G, McFawn L-A, Chalmers KJ, Li C (2019) Fine mapping of qGL5H, a major grain length locus in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 132, 883–893.
| Fine mapping of qGL5H, a major grain length locus in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 30465063PubMed |
Watt C, Zhou G, McFawn L-A, Li C (2020) Fine mapping qGL2H, a major locus controlling grain length in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 133, 2095–2103.
| Fine mapping qGL2H, a major locus controlling grain length in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 32193568PubMed |
Wendt T, Holme I, Dockter C, Preuß A, Thomas W, Druka A, Waugh R, Hansson M, Braumann I (2016) HvDep1 is a positive regulator of culm elongation and grain size in barley and impacts yield in an environment-dependent manner. PLoS One 11, e0168924
| HvDep1 is a positive regulator of culm elongation and grain size in barley and impacts yield in an environment-dependent manner.Crossref | GoogleScholarGoogle Scholar | 28005988PubMed |
Yang J, Yan R, Roy A, Xu D, Poisson J, Zhang Y (2015) The I-TASSER Suite: protein structure and function prediction. Nature Methods 12, 7–8.
| The I-TASSER Suite: protein structure and function prediction.Crossref | GoogleScholarGoogle Scholar | 25549265PubMed |
Ying J-Z, Ma M, Bai C, Huang X-H, Liu J-L, Fan Y-Y, Song X-J (2018) TGW3, a major qtl that negatively modulates grain length and weight in rice. Molecular Plant 11, 750–753.
| TGW3, a major qtl that negatively modulates grain length and weight in rice.Crossref | GoogleScholarGoogle Scholar | 29567450PubMed |
Zhang X, Wang J, Huang J, Lan H, Wang C, Yin C, Wu Y, Tang H, Qian Q, Li J, Zhang H (2012) Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proceedings of the National Academy of Sciences of the United States of America 109, 21534–21539.
| Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice.Crossref | GoogleScholarGoogle Scholar | 23236132PubMed |
Zhang D, Zhang M, Zhou Y, Wang Y, Shen J, Chen H, Zhang L, Lü B, Liang G, Liang J (2019) The rice G protein γ subunit DEP1/qPE9-1 positively regulates grain-filling process by increasing auxin and cytokinin content in rice grains. Rice 12, 91–102.
| The rice G protein γ subunit DEP1/qPE9-1 positively regulates grain-filling process by increasing auxin and cytokinin content in rice grains.Crossref | GoogleScholarGoogle Scholar | 31844998PubMed |
