Induced variation in BRASSINOSTEROID INSENSITIVE 1 (BRI1) confers a compact wheat architecture

. 2025 May 26 ; 25 (1) : 700. [epub] 20250526

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40419954

Grantová podpora
contract number 18187 Future Food International DTP agreement
contract number 18187 Future Food International DTP agreement
contract number 18187 Future Food International DTP agreement
Delivering Sustainable Wheat (BB/X011003/1) and Designing Future Wheat (BB/P016855/1) Biotechnology and Biological Sciences Research Council - United Kingdom
Delivering Sustainable Wheat (BB/X011003/1) and Designing Future Wheat (BB/P016855/1) Biotechnology and Biological Sciences Research Council - United Kingdom
Delivering Sustainable Wheat (BB/X011003/1) and Designing Future Wheat (BB/P016855/1) Biotechnology and Biological Sciences Research Council - United Kingdom
Delivering Sustainable Wheat (BB/X011003/1) and Designing Future Wheat (BB/P016855/1) Biotechnology and Biological Sciences Research Council - United Kingdom
Delivering Sustainable Wheat (BB/X011003/1) and Designing Future Wheat (BB/P016855/1) Biotechnology and Biological Sciences Research Council - United Kingdom
Towards Next Generation Crops' No. CZ.02.01.01/00/22_008/0004581), www.tangenc.cz European Regional Developmental Fund
Towards Next Generation Crops' No. CZ.02.01.01/00/22_008/0004581), www.tangenc.cz European Regional Developmental Fund

Odkazy

PubMed 40419954
PubMed Central PMC12105372
DOI 10.1186/s12870-025-06762-w
PII: 10.1186/s12870-025-06762-w
Knihovny.cz E-zdroje

BACKGROUND: The brassinosteroid (BR) plant hormones regulate numerous developmental processes, including those determining stem height, leaf angle, and grain size that have agronomic relevance in cereals. Indeed, barley (Hordeum vulgare) varieties containing uzu alleles that impair BR perception through mutations in the BR receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) exhibit a semi-dwarf growth habit and more upright leaves suitable for high-density planting. We used forward and reverse genetic approaches to develop novel BRI1 alleles in wheat (Triticum aestivum L.) and investigated their potential for crop productivity improvement. RESULTS: The combination of ethyl methanesulfonate-induced mutations introducing premature stop codons in all three homoeologous TaBRI1 genes resulted in severe dwarfism, malformed leaves and sterility as observed in bri1 mutants in other species. Double mutants had reduced flag-leaf angles (FLAs) conferring a more upright canopy but exhibited no differences in height or grain weight. In a targeted forward genetics screen using a double mutant, we identified two BR-insensitive lines with reduced height and FLA that contained amino acid substitutions in conserved regions of BRI-A1. The less severe mutant had a 56% reduction in FLA and was 35% shorter than the wild type, although seed set, seed area and grain weights were also reduced. The most severe mutants contained elevated levels of bioactive BRs and increased expression of BR-biosynthesis genes consistent with reduced feedback suppression of biosynthesis. CONCLUSION: Our study gives a better understanding of BRI1 function in wheat and provides mutants that could potentially be explored for improving grain yields when sown at high density.

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Yokota T, Arima M, Takahashi N. Castasterone, a new phytosterol with plant-hormone potency, from chestnut insect gall. Tetrahedron Lett. 1982;23:1275–8.

Divi UK, Krishna P. Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. Nat Biotechnol. 2009;26:131–6. PubMed

Tong H, Chu C. Functional specificities of brassinosteroid and potential utilization for crop improvement. Trends Plant Sci. 2018;23:1016–28. PubMed

Li J, Hee Nam K, Vafeados D, Chory J. BIN2, a new brassinosteroid-insensitive locus in arabidopsis. Plant Physiol. 2001;127:14–22. PubMed PMC

Li J, Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 1997;90:929–38. PubMed

Zhu J-Y, Sae-Seaw J, Wang Z-Y. Brassinosteroid signalling. Development. 2013;140:1615–20. PubMed PMC

Mathur J, Molnár G, Fujioka S, Takatsuto S, Sakurai A, Yokota T, et al. Transcription of the Arabidopsis CPD gene, encoding a steroidogenic cytochrome P450, is negatively controlled by brassinosteroids. Plant J. 1998;14:593–602. PubMed

Tanaka K, Asami T, Yoshida S, Nakamura Y, Matsuo T, Okamoto S. Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiol. 2005;138:1117–25. PubMed PMC

Sun Y, Fan X-Y, Cao D-M, Tang W, He K, Zhu J-Y, et al. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell. 2010;19:765–77. PubMed PMC

Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, et al. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J. 2011;65:634–46. PubMed

Wang Z-Y, Nakano T, Gendron J, He J, Chen M, Vafeados D, et al. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell. 2002;2:505–13. PubMed

Yin Y, Wang Z-Y, Mora-Garcia S, Li J, Yoshida S, Asami T, et al. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell. 2002;109:181–91. PubMed

He J-X, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, et al. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science. 2005;307:1634–8. PubMed PMC

Navarro C, Moore J, Ott A, Baumert E, Mohan A, Gill KS, et al. Evolutionary, comparative and functional analyses of the brassinosteroid receptor gene, BRI1, in wheat and its relation to other plant genomes. PLoS ONE. 2015;10:e0127544. PubMed PMC

Nakamura A, Fujioka S, Sunohara H, Kamiya N, Hong Z, Inukai Y, et al. The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol. 2006;140:580–90. PubMed PMC

Morinaka Y, Sakamoto T, Inukai Y, Agetsuma M, Kitano H, Ashikari M, et al. Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production of rice. Plant Physiol. 2006;141:924–31. PubMed PMC

Saisho D, Tanno K, Chono M, Honda I, Kitano H, Takeda K. Spontaneous brassinolide-insensitive barley mutants ‘uzu’ adapted to East Asia. Breed Sci. 2004;54:409–16.

Miyake K. Genetic studies in barley. I Bot Mag Tokyo. 1922;36:25–38.

Chono M, Honda I, Zeniya H, Yoneyama K, Saisho D, Takeda K, et al. A semidwarf phenotype of barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiol. 2003;133:1209–19. PubMed PMC

Takahashi R, Yamamoto J, Maruhashi W. Studies on the classification and the geographical distribution of the barley varieties.: IV. Linkage relation and the origin of the uzu or semibrachytic character. Japan J Crop Sci. 1951;20:167–70.

Jing Z, Wanxia Z. Tracing sources of dwarfing genes in barley breeding in China. Euphytica. 2003;131:285–93.

Fang J, Zhu W, Tong Y. Knock-down the expression of brassinosteroid receptor TaBRI1 reduces photosynthesis, tolerance to high light and high temperature stresses and grain yield in wheat. Plants. 2020;9:840. PubMed PMC

Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, et al. Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA. 2017;114:E913–21. PubMed PMC

Chen Y, Liang H, Ma X, Lou S, Xie Y, Liu Z, et al. An efficient rice mutagenesis system based on suspension-cultured cells. J Integr Plant Biol. 2013;55:122–30. PubMed

Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, et al. A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol. 2009;9:1–14. PubMed PMC

Tarkowská D, Novák O, Oklestkova J, Strnad M. The determination of 22 natural brassinosteroids in a minute sample of plant tissue by UHPLC–ESI–MS/MS. Anal Bioanal Chem. 2016;408:6799–812. PubMed

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. PubMed PMC

Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21. PubMed PMC

Putri GH, Anders S, Pyl PT, Pimanda JE, Zanini F. Analysing high-throughput sequencing data in Python with HTSeq 2.0. Bioinformatics. 2022;38:2943–5. PubMed PMC

Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:1–21. PubMed PMC

Ptošková K, Szecówka M, Jaworek P, Tarkowská D, Petřík I, Pavlović I, et al. Changes in the concentrations and transcripts for gibberellins and other hormones in a growing leaf and roots of wheat seedlings in response to water restriction. BMC Plant Biol. 2022;22:284. PubMed PMC

Hou L, Zhang A, Wang R, Zhao P, Zhang D, Jiang Y, et al. Brassinosteroid regulates root development with highly redundant genes in hexaploid wheat. Plant Cell Physiol. 2019;60:1761–77. PubMed

Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, et al. Heatmapper: web-enabled heat mapping for all. Nucl Acids Res. 2016;44:W147–53. PubMed PMC

Oliveros JC, Venny C. An interactive tool for comparing lists with Venn’s diagrams. BioinfoGP, CNB-CSIC. 2007.

Reimand J, Arak T, Adler P, Kolberg L, Reisberg S, Peterson H, et al. g: Profiler—a web server for functional interpretation of gene lists (2016 update). Nucl Acids Res. 2016;44:W83–9. PubMed PMC

Li H-Y, Wang H-M, Jang S. Rice lamina joint inclination assay. Bio Protoc. 2017;7:e2409–e2409. PubMed PMC

Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, et al. Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell. 2000;12:1591–605. PubMed PMC

Dockter C, Gruszka D, Braumann I, Druka A, Druka I, Franckowiak J, et al. Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the green revolution genetic toolkit. Plant Physiol. 2014;166:1912–27. PubMed PMC

Clouse SD, Langford M, McMorris TC. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 1996;111:671–8. PubMed PMC

Tian J, Wang C, Chen F, Qin W, Yang H, Zhao S, et al. Maize smart-canopy architecture enhances yield at high densities. Nature. 2024;632:576–84. PubMed

Zhang X, Meng W, Liu D, Pan D, Yang Y, Chen Z, et al. Enhancing rice panicle branching and grain yield through tissue-specific brassinosteroid inhibition. Science. 2024;383:eadk8838. PubMed

Song L, Liu J, Cao B, Liu B, Zhang X, Chen Z, et al. Reducing brassinosteroid signalling enhances grain yield in semi-dwarf wheat. Nature. 2023;617:118–24. PubMed PMC

Lyu J, Wang D, Sun N, Yang F, Li X, et al. The TaSnRK1-TabHLH489 module integrates brassinosteroid and sugar signalling to regulate the grain length in bread wheat. Plant Biotech J. 2024;22:1989–2006. PubMed PMC

Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson I, et al. Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature. 2011;474:467–71. PubMed PMC

She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, et al. Structural insight into brassinosteroid perception by BRI1. Nature. 2011;474:472–6. PubMed PMC

Sun C, Yan K, Han JT, Tao, Lv MH, Shi T, et al. Scanning for new BRI1 mutations via TILLING analysis. Plant Physiol. 2017; 174:1881–96. PubMed PMC

Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M. Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. Plant J. 2014;78:31–43. PubMed PMC

Oh MH, Ray WK, Huber SC, Asara JM, Gage DA, Clouse SD. Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 2000;124:751–66. PubMed PMC

Vert G, Nemhauser JL, Geldner N, Hong F, Chory J. Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol. 2005;21:177–201. PubMed

Yan L, Ma Y, Liu D, Wei X, Sun Y, Chen X, et al. Structural basis for the impact of phosphorylation on the activation of plant receptor-like kinase BAK1. Cell Res. 2012;22:1304–8. PubMed PMC

Janeczko A, Swaczynová J. Endogenous brassinosteroids in wheat treated with 24-epibrassinolide. Biol Plant. 2010;54:477–82.

Kim BK, Fujioka S, Takatsuto S, Tsujimoto M, Choe S. Castasterone is a likely end product of brassinosteroid biosynthetic pathway in rice. Biochem Biophys Res Commun. 2008;374:614–9. PubMed

Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA. The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell. 1998;10:231–43. PubMed PMC

Ohnishi T, Godza B, Watanabe B, Fujioka S, Hategan L, Ide K, et al. CYP90A1/CPD, a brassinosteroid biosynthetic cytochrome P450 of Arabidopsis, catalyzes C-3 oxidation. J Biol Chem. 2012;287:31551–60. PubMed PMC

Choe S. Signal-transduction pathways toward the regulation of brassinosteroid biosynthesis. J Plant Biol. 2007;50:225–9.

Ye H, Li L, Yin Y. Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J Integr Plant Biol. 2011;53:455–68. PubMed

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