Parallel tuning of semi-dwarfism via differential splicing of Brachytic1 in commercial maize and smallholder sorghum.
RNA-Seq
crop evolution
gene regulation
genome-wide association study
plant architecture
plant hormones
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
27
03
2023
accepted:
19
08
2023
medline:
3
11
2023
pubmed:
22
9
2023
entrez:
22
9
2023
Statut:
ppublish
Résumé
In the current genomic era, the search and deployment of new semi-dwarf alleles have continued to develop better plant types in all cereals. We characterized an agronomically optimal semi-dwarf mutation in Zea mays L. and a parallel polymorphism in Sorghum bicolor L. We cloned the maize brachytic1 (br1-Mu) allele by a modified PCR-based Sequence Amplified Insertion Flanking Fragment (SAIFF) approach. Histology and RNA-Seq elucidated the mechanism of semi-dwarfism. GWAS linked a sorghum plant height QTL with the Br1 homolog by resequencing a West African sorghum landraces panel. The semi-dwarf br1-Mu allele encodes an MYB transcription factor78 that positively regulates stalk cell elongation by interacting with the polar auxin pathway. Semi-dwarfism is due to differential splicing and low functional Br1 wild-type transcript expression. The sorghum ortholog, SbBr1, co-segregates with the major plant height QTL qHT7.1 and is alternatively spliced. The high frequency of the Sbbr1 allele in African landraces suggests that African smallholder farmers used the semi-dwarf allele to improve plant height in sorghum long before efforts to introduce Green Revolution-style varieties in the 1960s. Surprisingly, variants for differential splicing of Brachytic1 were found in both commercial maize and smallholder sorghum, suggesting parallel tuning of plant architecture across these systems.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1930-1943Subventions
Organisme : Bill & Melinda Gates Foundation
ID : INV-009319
Pays : United States
Organisme : Bill & Melinda Gates Foundation
ID : INV-009319
Pays : United States
Informations de copyright
© 2023 Corteva Agriscience. New Phytologist © 2023 New Phytologist Foundation.
Références
Bage SA, Barten TJ, Brown AN, Crowley JH, Deng M, Fouquet R, Gomez JR, Hatton TW, Lamb JC, LeDeaux JR et al. 2020. Genetic characterization of novel and CRISPR-Cas9 edited maize brachytic2 alleles. Plant Gene 21: 100198.
Bensen RJ, Johal GS, Crane VC, Tossberg JT, Schnable PS, Meeley RB, Briggs SP. 1995. Cloning and characterization of the maize AN1 gene. Plant Cell 7: 75-84.
Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J et al. 2007. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19: 131-147.
Bosch M, Mayer C-D, Cookson A, Donnison IS. 2011. Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. Journal of Experimental Botany 62: 3545-3561.
Bouchet S, Olatoye MO, Marla SR, Perumal R, Tesso T, Yu J, Tuinstra M, Morris GP. 2017. Increased power to dissect adaptive traits in global sorghum diversity using a Nested Association Mapping population. Genetics 206: 573-585.
Brenton ZW, Cooper EA, Myers MT, Boyles RE, Shakoor N, Zielinski KJ, Rauh BL, Bridges WC, Morris GP, Kresovich S. 2016. A genomic resource for the development, improvement, and exploitation of sorghum for bioenergy. Genetics 204: 21-33.
Browning BL, Zhou Y, Browning SR. 2018. A one-penny imputed genome from next-generation reference panels. The American Journal of Human Genetics 103: 338-348.
Dahlberg JA, Burke JJ, Rosenow DT. 2004. Development of a sorghum core collection: refinement and evaluation of a subset from Sudan. Economic Botany 58: 556-567.
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM et al. 2021. Twelve years of SAMtools and BCFtools. GigaScience 10: giab008.
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. Star: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
Eshed Y, Lippman ZB. 2019. Revolutions in agriculture chart a course for targeted breeding of old and new crops. Science 366: eaax0025.
Faye JM, Maina F, Akata EA, Sine B, Diatta C, Mamadou A, Marla S, Bouchet S, Teme N, Rami JF et al. 2021. A genomics resource for genetics, physiology, and breeding of West African sorghum. The Plant Genome 14: e20075.
Fisher RA. 1930. The genetical theory of natural selection. Oxford, UK: Oxford University Press.
Forestan C, Farinati S, Varotto S. 2012. The maize PIN gene family of auxin transporters. Frontiers in Plant Science 3: 1-23.
George-Jaeggli B, Jordan DR, van Osterom EJ, Hammer GL. 2011. Decrease in sorghum grain yield due to the dw3 dwarfing gene is caused by reduction in shoot biomass. Field Crops Research 124: 231-239.
Gomez FE, Mullet JE, Muliana AH, Niklas KJ, Rooney WL. 2020. The genetic architecture of biomechanical traits in sorghum. Crop Science 60: 82-99.
Gomez MD, Urbez C, Perez-Amador MA, Carbonell J. 2011. Characterization of constricted fruit (ctf) mutant uncovers a role for AtMYB117/LOF1 in ovule and fruit development in Arabidopsis thaliana. PLoS ONE 6: e18760.
Hashimoto S, Wake T, Nakamura H, Minamiyama M, Araki-Nakamura S, Ohmae-Shinohara K, Koketsu E, Okamura S, Miura K, Kawaguchi H et al. 2021. The dominance model for heterosis explains culm length genetics in a hybrid sorghum variety. Science Reporter 11: 4532.
Hedden P. 2003. The genes of the Green Revolution. Trends in Genetics 19: 5-9.
Hu Z, Olatoye M, Marla S, Morris G. 2019. An integrated genotyping by sequencing polymorphism map for over 10,000 sorghum genotypes. Plant Genome 12: 180044.
Jiao S, Hazebroek JP, Chamberlin MA, Perkins M, Sandhu AS, Gupta R, Simcox KD, Yinghong L, Prall A, Heetland L et al. 2019. Chitinase-like1 plays a role in stalk tensile strength in maize. Plant Physiology 181: 1127-1147.
Kante M, Chepken C, Oboko R. 2018. Effects of farmers' peer influence on the use of ICT-based farm input information in developing countries: a case in Sikasso, Mali. Journal of Digital Media & Interaction 1: 99-116.
Kempton H. 1920. Heritable characters of maize. III. Brachytic culms. Journal of Heredity 11: 317-322.
Khush GS. 2001. Green revolution: the way forward. Nature Reviews Genetics 2: 815-822.
Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK. 2012. Varscan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Research 22: 568-576.
LeBauer D, Maxwell B, Demieville J, Fahlgren N, French A, Garnett R, Hu Z, Huynh K, Kooper R, Li Z et al. 2020. Data from: TERRA-REF, an open reference data set from high resolution genomics, phenomics, and imaging sensors. Dryad. doi: 10.5061/dryad.4b8gtht99.
Lee DK, Geisler M, Springer PS. 2009. LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136: 2423-2432.
Li H, Durbin R. 2010. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
Li X, Li X, Fridman E, Tesso TT, Yu J. 2015. Dissecting repulsion linkage in the dwarfing gene Dw3 region for sorghum plant height provides insights into heterosis. Proceedings of the National Academy of Sciences, USA 112: 11823-11828.
McCormick RF, Truong SK, Sreedasyam A, Jenkins J, Shu S, Sims D, Kennedy M, Amir Ebrahimi M, Weers BD, McKinley B et al. 2018. The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. The Plant Journal 93: 338-354.
Monk R, Franks C, Dahlberg J. 2014. Sorghum. In: Smith S, ed. Yield gains in major U.S. field crops. Madison, WI, USA: CSSA Special Publications, 293-310.
Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS. 2003. Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302: 81-84.
Multani DS, Meeley RB, Paterson AH, Gray J, Briggs SP, Johal GS. 1998. Plant-pathogen microevolution: molecular basis for the origin of a fungal disease in maize. Proceedings of the National Academy of Sciences, USA 95: 1686-1691.
Muszynski MG, Dam T, Li B, Shirbroun DM, Hou Z, Bruggemann E, Archibald R, Ananiev EV, Danilevskaya ON. 2006. delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiology 142: 1523-1536.
National Research Council. 1996. Lost crops of Africa: volume I: grains. Washington, D.C., USA: The National Academies Press.
Ndjeunga J, Mausch K, Simtowe F. 2015. Assessing the effectiveness of agricultural R&D for groundnut, pearl millet, pigeon pea and sorghum in West and Central Africa and East and Southern Africa. In: Walker TS, Alwang J, eds. Crop improvement, adoption, and impact of improved varieties in food crops in Sub-Saharan Africa. Wallingford, UK: CABI Books, 123-147.
Neuffer MG, Coe EH, Wessler SR. 1997. Mutants of maize. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
Ogihara Y, Takumi S, Handa H. 2015. Advances in wheat genetics: from genome to field, proceedings of the 12th international wheat genetics symposium. New York, NY, USA: Springer Open.
Orr HA. 2005. The genetic theory of adaptation: a brief history. Nature Reviews Genetics 6: 119-127.
Paque S, Mouille G, Grandont L, Alabadí D, Gaertner C, Goyallon A, Muller P, Primard-Brisset C, Sormani R, Blázquez MA et al. 2014. AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in Arabidopsis. Plant Cell 26: 280-295.
Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. 2017. Salmon: fast and bias-aware quantification of transcript expression using dual-phase inference. Nature Methods 14: 417-419.
Peiffer JA, Romay MC, Gore MA, Flint-Garcia SA, Zhang Z, Millard MJ, Gardner CA, McMullen MD, Holland JB, Bradbury PJ et al. 2014. The genetic architecture of maize height. Genetics 196: 1337-1356.
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F et al. 1999. “Green revolution” genes encode mutant gibberellin response modulators. Nature 400: 256-261.
Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL. 2015. Stringtie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology 33: 290-295.
Rambaut A. 2009. FigTree v.1.2.2. Edinburgh, UK: Institute of Evolution Biology, University of Edinburgh.
Soyk S, Müller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jiménez-Gómez JM, Lippman ZB. 2017. Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nature Genetics 49: 162-168.
Spielmeyer W, Ellis MH, Chandler PM. 2002. Semi-dwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences, USA 99: 9043-9048.
Stitzer MC, Ross-Ibarra J. 2018. Maize domestication and gene interaction. New Phytologist 220: 395-408.
Sun S, Zhou Y, Lai J. 2018. Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nature Genetics 50: 1289-1295.
Thompson JD, Higgins DG, Gibson TJ. 1994. ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673-4680.
Xin Z, Wang M, Cuevas HE, Chen J, Harrison M, Pugh NA, Morris G. 2021. Sorghum genetics, genomics, and breeding resources. Planta 254: 114.