Genome-wide dissection of genes shaping inflorescence morphology in 242 Chinese south-north sorghum accessions.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
28 10 2024
Historique:
received: 30 04 2024
accepted: 15 10 2024
medline: 29 10 2024
pubmed: 29 10 2024
entrez: 29 10 2024
Statut: epublish

Résumé

The inflorescences morphology (IM) of sorghum (Sorghum bicolor L. Moench) affects its resistance to pests, diseases, and grain yields. However, the specific genetic factors underlying in IM are not yet fully elucidated. Here we conducted a comprehensive genome-wide association analysis (GWAS) to identify the stable and adaptive Quantitative Trait Loci (QTL) for five IM traits (panicle length, the number of cob nodes, the number of primary branches, the largest length of the primary branch, and panicle type) in a sorghum panel, which adapted to different environments from the south to north in China. Totally, 2,015,850 high quality single nucleotide polymorphisms (SNPs) were obtained. Population structure analysis showed that two distinct genetic sub-populations were divided according to their geographic origin. Seventy-one QTLs distributed in 41 genetic regions on 9 chromosomes were identified. These regions harbored 21 high-confident candidate genes that were homologous to rice domestication genes, including 7 related to IM. Two domestication-related genes (Sobic.003G052700 and Sobic.006G247700) were located into two major QTL regions (QTL3.4721839 and QTL6.58709500) which were identified in multi-environments. Allelic variations in the two genes displayed a geographical pattern, indicating that different IM traits were selected by south and north sorghum breeders, such as south sorghums had long and loose panicles in order to adapt the hot and humid climate, while north sorghums had short and compact panicle to increase planting density and grain yield per unit area due to dry climate. This work provides new breeding strategies and resources for developing locally adapted sorghum varieties.

Identifiants

pubmed: 39468118
doi: 10.1038/s41598-024-76568-7
pii: 10.1038/s41598-024-76568-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

25828

Subventions

Organisme : This study was supported by National Key R&D Program of China
ID : 2018YFD1000706/2018YFD10007011
Organisme : National Natural Science Foundation of China
ID : 32172036, 31571681
Organisme : Zhejiang Major Scientific and Technological Project of Agricultural (Upland crop) Breeding ,and Zhejiang Key Laboratory of Digital Dry Land Crops
ID : 2021C02064-6,2022E10012
Organisme : Guizhou Provincial Science and Technology Plan Project, Innovation Capacity Building Project of Guizhou Scientific Institutions, Guizhou Academy of Agricultural Sciences Key Laboratory Project for Crop Gene Resources and Germplasm Innovation in Karst Mountain regions
ID : QKHS [2022]key026, QKFQ[2022]007],QNKZZZY(2023)06

Informations de copyright

© 2024. The Author(s).

Références

Doebley, J. F., Gaut, B. S. & Smith, B. D. The molecular genetics of crop domestication. Cell 127(7), 1309–1321 (2006).
pubmed: 17190597 doi: 10.1016/j.cell.2006.12.006
Bell, A. D. Plant Form: An Illustrated Guide to Flowering Plant Morphology (Timber Press Inc., 2008).
Brown, P. J. et al. Inheritance of inforescence architecture in sorghum. Theor. Appl. Genet. 113, 931–942 (2006).
pubmed: 16847662 doi: 10.1007/s00122-006-0352-9
Takanashi, H. et al. Genetic dissection of QTLs associated with spikelet-related traits and grain size in sorghum. Sci. Rep. 11, 9398–9414 (2021).
pubmed: 33931706 pmcid: 8087780 doi: 10.1038/s41598-021-88917-x
Gladman, N. et al. Fertility of pedicellate spikelets in sorghum is controlled by a Jasmonic Acid regulatory module. Int J Mol Sci. 20(19), 4951. https://doi.org/10.3390/ijms20194951 (2019).
doi: 10.3390/ijms20194951 pubmed: 31597271 pmcid: 6801740
Doggett, H. Sorghum 2nd edn. (Longmans Scientific and Technical, 1988).
Harlan, J. R. & de Wet, J. M. A simplified classification of cultivated sorghum. Crop Sci. 12, 172–176 (1972).
doi: 10.2135/cropsci1972.0011183X001200020005x
Smith, C. W. & Frederiksen, R. A. Sorghum: Origin, History, Technology, and Production 824 (John Wiley and Sons, 2000).
Dillon, S. L. et al. Domestication to crop improvement: Genetic resources for Sorghum and Saccharum (Andropogoneae). Ann. Bot. 100, 975–989. https://doi.org/10.1093/aob/mcm192 (2007).
doi: 10.1093/aob/mcm192 pubmed: 17766842 pmcid: 2759214
House, L. R. A Guide to Sorghum Breeding 2nd edn. (International Crops Research Institute for the Semi-Arid Tropics, 1985).
Kimber, C. T. Chapter 1.1: Origin of domesticated sorghum and its early diffusion to India and China. In Sorghum: Origin, History, Technology and Production (eds Smith, C. W. & Frederiksen, R. A.) 3–98 (John Wiley and Sons, Inc, 2008).
OGTR. The Biology of Sorghum bicolor (L.) Moench subsp. bicolor (Sorghum). Australian Government Office of the Gene Technology Regulator. https://www.ogtr.gov.au/sites/default/files/files/2021-07/the_biology_of_sorghum.pdf (2017)
Desmae, H., Jordan, D. R. & Godwin, I. D. Geographic patterns of phenotypic diversity in sorghum [Sorghum bicolor (L.) Moench] landraces from North Eastern Ethiopia. Afr. J. Agri. Res. 11, 3111–3122. https://doi.org/10.5897/AJAR2016.11121 (2016).
doi: 10.5897/AJAR2016.11121
Lasky, J. R. et al. Genome-environment associations in sorghum landraces predict adaptive traits. Sci. Adv. 1, e1400218 (2015).
pubmed: 26601206 pmcid: 4646766 doi: 10.1126/sciadv.1400218
Olatoye, M. O., Hu, Z., Maina, F. & Morris, G. P. Genomic signatures of adaptation to a precipitation gradient in Nigerian sorghum. G3 Genes Genomes Genet. 8, 3269–3281 (2018).
doi: 10.1534/g3.118.200551
Qiao, K. D. & Wei, Z. S. (eds) Varieties of Sorghum in China. In Chinese, 2 vols. Edited by Liaoning Agricultural Institute (Agricultural Publishing, Beijing, China 1978, 1981).
Morris, G. P. et al. Population genomic and genome-wide association studies of agroclimatic traits in sorghum. Proc. Natl. Acad. Sci. 110, 453–458 (2013).
pubmed: 23267105 doi: 10.1073/pnas.1215985110
Witt Hmon, K. P., Shehzad, T. & Okuno, K. Variation in inflorescence architecture associated with yield components in a sorghum germplasm. Plant Genet. Resour. 11, 258–265 (2013).
doi: 10.1017/S1479262113000154
Chen, W. K. et al. Convergent selection of a WD40 protein that enhances grain yield in maize and rice. Science 375, 1372–1383 (2022).
doi: 10.1126/science.abg7985
Vavilov, N. I. The law of homologous series in variation. J. Genet. 12, 47–89 (1922).
doi: 10.1007/BF02983073
Hermann, K. & Kuhlemeier, C. The genetic architecture of natural variation in flower morphology. Curr. Opin. Plant Biol. 14, 60–65 (2011).
pubmed: 20934369 doi: 10.1016/j.pbi.2010.09.012
Zhang, D. & Yuan, Z. Molecular control of grass inflorescence development. Annu. Rev. Plant Biol. 65, 553–578. https://doi.org/10.1146/annurev-arplant-050213-040104 (2014).
doi: 10.1146/annurev-arplant-050213-040104 pubmed: 24471834
Ikeda-Kawakatsu, K. et al. Expression level of ABERRANT PANICLE ORGANIZATION1 determines rice inflorescence form through control of cell proliferation in the meristem. Plant Physiol. 150, 736–747 (2009).
pubmed: 19386809 pmcid: 2689948 doi: 10.1104/pp.109.136739
Ookawa, T. et al. New approach for rice improvement using a pleiotropic QTL gene for lodging resistance and yield. Nat. Commun. 1, 132 (2010).
pubmed: 21119645 doi: 10.1038/ncomms1132
Miura, K. et al. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545–549. https://doi.org/10.1038/ng.592 (2010).
doi: 10.1038/ng.592 pubmed: 20495564
Bai, X. F. et al. Regulatory role of FZP in the determination of panicle branching and spikelet formation in rice. Sci. Rep. 6, 19022 (2016).
pubmed: 26744119 pmcid: 4705600 doi: 10.1038/srep19022
Fujishiro, Y. et al. Comprehensive panicle phenotyping reveals that qSrn7/FZP influences higher-order branching. Sci. Rep. 8(1), 12511. https://doi.org/10.1038/s41598-018-30395-9 (2018).
doi: 10.1038/s41598-018-30395-9 pubmed: 30131566 pmcid: 6104091
Komatsu, M., Chujo, A., Nagato, Y., Shimamoto, K. & Kyozuka, J. FRIZZY PANICLE is required to prevent the formation of axillary meristems and to establish floral meristem identity in rice spikelets. Development 130, 3841–3850. https://doi.org/10.1242/dev.00564 (2003).
doi: 10.1242/dev.00564 pubmed: 12835399
Huang, X. Z. et al. Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41(4), 494–497 (2009).
pubmed: 19305410 doi: 10.1038/ng.352
Agata, A. et al. Diverse panicle architecture results from various combinations of Prl5/GA20ox4 and Pbl6/APO1 alleles. Commun. Biol. 3(1), 302. https://doi.org/10.1038/s42003-020-1036-8 (2020).
doi: 10.1038/s42003-020-1036-8 pubmed: 32528064 pmcid: 7289860
Zhang, L. Y. et al. GWAS of grain color and tannin content in Chinese sorghum based on whole-genome sequencing. Theor. Appl. Genet. 136, 77 (2023).
pubmed: 36952041 pmcid: 10036430 doi: 10.1007/s00122-023-04307-z
Tao, Y. F. et al. Novel grain weight loci revealed in a cross between cultivated and wild Sorghum. Plant Genome 11, 1–10 (2018).
doi: 10.3835/plantgenome2017.10.0089
Tao, Y. et al. Large-scale GWAS in sorghum reveals common genetic control of grain size among cereals. Plant Biotechnol. J. 18(4), 1093–1105 (2020).
pubmed: 31659829 doi: 10.1111/pbi.13284
Bouchet, S. et al. Increased power to dissect adaptive traits in global sorghum diversity using a nested association mapping population. Genetics 206, 573–585 (2017).
pubmed: 28592497 pmcid: 5499173 doi: 10.1534/genetics.116.198499
Murphy, R. L. et al. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc. Natl. Acad. Sci. U.S.A. 108, 16469–16474 (2011).
pubmed: 21930910 pmcid: 3182727 doi: 10.1073/pnas.1106212108
Thurber, C. S., Ma, J. M., Higgins, R. H. & Brown, P. J. Retrospective genomic analysis of sorghum adaptation to temperate-zone grain production. Genome Biol. 14, R68 (2013).
pubmed: 23803286 pmcid: 3706989 doi: 10.1186/gb-2013-14-6-r68
Shehzad, T. & Okuno, K. QTL mapping for yield and yield-contributing traits in sorghum (Sorghum bicolor (L.) Moench) with genome-based SSR markers. Euphytica 203, 17–31 (2015).
doi: 10.1007/s10681-014-1243-9
Zhang, D. et al. Genetic analysis of inflorescence and plant height components in sorghum (Panicoidae) and comparative genetics with rice (Oryzoidae). BMC Plant Biol. 15, 107. https://doi.org/10.1186/s12870-015-0477-6 (2015).
doi: 10.1186/s12870-015-0477-6 pubmed: 25896918 pmcid: 4404672
Parh, D. DNA-Based Markers for Ergot Resistance in Sorghum. PhD thesis, University of Queensland (2005).
Rami, J. F. et al. Quantitative trait loci for grain quality, productivity, morphological and agronomical traits in sorghum (Sorghum bicolor L. Moench). Theor. Appl. Genet. 97, 605–616 (1998).
doi: 10.1007/s001220050936
Sakhi, S., Shehzad, T., Rehman, S. & Okuno, K. Mapping the QTLs underlying drought stress at developmental stage of sorghum (Sorghum bicolor (L.) Moench) by association analysis. Euphytica 193, 433–450 (2013).
doi: 10.1007/s10681-013-0963-6
Koppolu, R., Chen, S. L. & Schnurbusch, T. Evolution of inflorescence branch modifications in cereal crops. Curr. Opin. Plant Biol. 65, 102168–102175 (2022).
pubmed: 35016076 doi: 10.1016/j.pbi.2021.102168
Kellogg, E. A. Evolutionary history of the grasses. Plant Physiol. 125, 1198–1205 (2001).
pubmed: 11244101 pmcid: 1539375 doi: 10.1104/pp.125.3.1198
Abbo, S. et al. Plant domestication versus crop evolution: A conceptual framework for cereals and grain legumes. Trends Plant Sci. 19, 351–360 (2014).
pubmed: 24398119 doi: 10.1016/j.tplants.2013.12.002
Yuan, Z., Persson, S. & Zhang, D. B. Molecular and genetic pathways for optimizing spikelet development and grain yield. Abiotech 1, 276–292 (2020).
pubmed: 36304128 pmcid: 9590455 doi: 10.1007/s42994-020-00026-x
Bommert, P. & Whipple, C. Grass inflorescence architecture and meristem determinacy. Semin. Cell Dev Biol. 79, 37–47 (2018).
pubmed: 29020602 doi: 10.1016/j.semcdb.2017.10.004
Ikeda-Kawakatsu, K., Ito, M., Nagasawa, N., Kyozuka, J. & Nagato, Y. Rice ABERRANT PANICLE ORGANIZATION 1, encoding an F-box protein, regulates meristem fate. Plant J. 51, 1030–1040 (2007).
doi: 10.1111/j.1365-313X.2007.03200.x
Koppolu, R. & Schnurbusch, T. Developmental pathways for shaping spike inflorescence architecture in barley and wheat. J. Integr. Plant Biol. 61, 278–295 (2019).
pubmed: 30609316 doi: 10.1111/jipb.12771
Vollbrecht, E., Springer, P. S., Goh, L., Buckler Iv, E. S. & Martienssen, R. Architecture of floral branch systems in maize and related grasses. Nature 436, 1119 (2005).
pubmed: 16041362 doi: 10.1038/nature03892
Wang, Y., Wang, Y., Song, S., Li, Z. & Wang, X. Genetic regulation of shoot architecture in cereals. Nat. Rev. Genet. 21(6), 430–444 (2020).
doi: 10.1038/nrm831
Zhou, Y., Xu, M., Wu, M. & Zhang, H. Rice MADS29 negatively regulates rice inflorescence meristem activity through controlling cytokinin level and WUS expression. BMC Plant Biol. 18(1), 1–9 (2018).
Je, B. I. et al. Signaling from maize organ primordia via the FASCIATED EAR3 receptor kinase controls stem cell proliferation and yield traits. Nat. Genet. 48(7), 785–791 (2016).
pubmed: 27182966 doi: 10.1038/ng.3567
Galli, M. et al. Auxin signaling modules regulate maize inflorescence architecture. Proc. Natl. Acad. Sci. 112(42), 13372–13377 (2015).
pubmed: 26464512 pmcid: 4629326 doi: 10.1073/pnas.1516473112
Li, S. et al. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature 560(7720), 595–600 (2019).
doi: 10.1038/s41586-018-0415-5
Bortiri, E. et al. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18, 574–585 (2006).
pubmed: 16399802 pmcid: 1383634 doi: 10.1105/tpc.105.039032
Claeys, H. et al. Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat. Plants 5, 352–357 (2019).
pubmed: 30936436 pmcid: 7444751 doi: 10.1038/s41477-019-0394-z
Gallavotti, A. et al. The control of axillary meristem fate in the maize ramosa pathway. Development 137, 2849–2856 (2010).
pubmed: 20699296 pmcid: 2938917 doi: 10.1242/dev.051748
Satoh-Nagasawa, N., Nagasawa, N., Malcomber, S., Sakai, H. & Jackson, D. Trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441, 227–230 (2006).
pubmed: 16688177 doi: 10.1038/nature04725
Ikeda-Kawakatsu, K., Maekawa, M., Izawa, T., Itoh, J. I. & Nagato, Y. ABERRANT PANICLE ORGANIZATION 2/RFL, the rice ortholog of Arabidopsis LEAFY, suppresses the transition from inflorescence meristem to floral meristem through interaction with APO1. Plant J. 69, 168–180 (2012).
pubmed: 21910771 doi: 10.1111/j.1365-313X.2011.04781.x
Huang, Y., Bai, X., Luo, M. & Xing, Y. Short Panicle 3 controls panicle architecture by upregulating APO2/RFL and increasing cytokinin content in rice. J. Integr. Plant Biol. 61, 987–999 (2019).
pubmed: 30302902 doi: 10.1111/jipb.12729
Huang, L. et al. The LARGE2-APO1/APO2 regulatory module controls panicle size and grain number in rice. Plant Cell. 33, 1212–1228 (2021).
pubmed: 33693937 doi: 10.1093/plcell/koab041
Poursarebani, N. et al. COMPOSITUM 1 contributes to the architectural implification of barley inflorescence via meristem identity signals. Nat. Commun. 11, 5138 (2020).
pubmed: 33046693 pmcid: 7550572 doi: 10.1038/s41467-020-18890-y
Poursarebani, N. et al. The genetic basis of composite spike form in barley and ‘Miracle-Wheat’. Genetics 201, 155–165 (2015).
pubmed: 26156223 pmcid: 4566260 doi: 10.1534/genetics.115.176628
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168 pmcid: 2705234 doi: 10.1093/bioinformatics/btp324
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43(5), 491–498 (2011).
pubmed: 21478889 pmcid: 3083463 doi: 10.1038/ng.806
Dong, S. S. et al. LDBlockShow: A fast and convenient tool for visualizing linkage disequilibrium and haplotype blocks based on variant call format files. Brief Bioinform. 22(4), bbaa227 (2021).
pubmed: 33126247 doi: 10.1093/bib/bbaa227
Li, X. K., Shi, Z. Y., Gao, J. H., Wang, X. C. & Guo, K. CandiHap: A haplotype analysis toolkit for natural variation study. Mol. Breed. 43, 21 (2023).
pubmed: 37313297 pmcid: 10248607 doi: 10.1007/s11032-023-01366-4
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158. https://doi.org/10.1093/bioinformatics/btr330 (2011).
doi: 10.1093/bioinformatics/btr330 pubmed: 21653522 pmcid: 3137218
Zou, G. H. et al. Sorghum qTGW1a encodes a G-protein subunit and acts as a negative regulator of grain size. J. Exp. Bot. 71(18), 5389–5401 (2020).
pubmed: 32497208 doi: 10.1093/jxb/eraa277
Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28(5), 511–515 (2010).
pubmed: 20436464 pmcid: 3146043 doi: 10.1038/nbt.1621

Auteurs

Guihua Zou (G)

Institute of Virology and Biotechnology, Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Zhejiang Key Laboratory of Digital Dry Land Crops, Hangzhou, 310021, China.

Yanqing Ding (Y)

Guizhou Institute of Upland Crops, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, China.

Jianxia Xu (J)

Guizhou Institute of Upland Crops, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, China.

Zhou Feng (Z)

Guizhou Institute of Upland Crops, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, China.

Ning Cao (N)

Guizhou Institute of Upland Crops, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, China.

Heyun Chen (H)

Institute of Virology and Biotechnology, Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Zhejiang Key Laboratory of Digital Dry Land Crops, Hangzhou, 310021, China.

Heqin Liu (H)

Institute of Virology and Biotechnology, Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Zhejiang Key Laboratory of Digital Dry Land Crops, Hangzhou, 310021, China.

Xueqiang Zheng (X)

Institute of Virology and Biotechnology, Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Zhejiang Key Laboratory of Digital Dry Land Crops, Hangzhou, 310021, China.

Xiuhui Liu (X)

Institute of Virology and Biotechnology, Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, Zhejiang Key Laboratory of Digital Dry Land Crops, Hangzhou, 310021, China.

Liyi Zhang (L)

Guizhou Institute of Upland Crops, Guizhou Academy of Agricultural Sciences, Guiyang, 550006, China. lyzhang1997@hotmail.com.

Articles similaires

Humans Neoplasms Male Female Middle Aged
Humans Macular Degeneration Mendelian Randomization Analysis Life Style Genome-Wide Association Study
Humans Male Female Aged Middle Aged

Classifications MeSH