Abstract
Key message
A novel locus on Agropyron cristatum chromosome 6P that increases grain number and spikelet number was identified in wheat–A. cristatum derivatives and across 3 years.
Abstract
Agropyron cristatum (2n = 4x = 28, PPPP), which has the characteristics of high yield with multiple flowers and spikelets, is a promising gene donor for wheat high-yield improvement. Identifying the genetic loci and genes that regulate yield could elucidate the genetic variations in yield-related traits and provide novel gene sources and insights for high-yield wheat breeding. In this study, cytological analysis and molecular marker analysis revealed that del10a and del31a were wheat–A. cristatum chromosome 6P deletion lines. Notably, del10a carried a segment of the full 6PS and 6PL bin (1–13), while del31a carried a segment of the full 6PS and 6PL bin (1–8). The agronomic characterization and genetic population analysis confirmed that the 6PL bin (9–13) brought about an increase in grain number per spike (average increase of 10.43 grains) and spikelet number per spike (average increase of 3.67) over the three growing seasons. Furthermore, through resequencing, a multiple grain number locus was mapped to the physical interval of 593.03–713.89 Mb on chromosome 6P of A. cristatum Z559. The RNA-seq analysis revealed the expression of 537 genes in the del10a young spike tissue, with the annotation indicating that 16 of these genes were associated with grain number and spikelet number. Finally, a total of ten A. cristatum-specific molecular markers were developed for this interval. In summary, this study presents novel genetic material that is useful for high-yield wheat breeding initiatives to meet the challenge of global food security through enhanced agricultural production.
Similar content being viewed by others
Abbreviations
- GNS:
-
Grain number per spike
- SNS:
-
Spikelet number per spike
- FFNS:
-
Fertile floret number per spikelet
- TGW:
-
Thousand-grain weight
- GISH:
-
Genomic in situ hybridization
- FISH:
-
Fluorescence in situ hybridization
References
An D, Zheng Q, Luo Q, Ma P, Zhang H, Li L, Han F, Xu H, Xu Y, Zhang X, Zhou Y (2015) Molecular cytogenetic identification of a new wheat–rye 6R chromosome disomic addition line with powdery mildew resistance. PLoS ONE 10:e0134534
Boden SA, Cavanagh C, Cullis BR, Ramm K, Greenwood J, Jean Finnegan E, Trevaskis B, Swain SM (2015) Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nat Plants 1:14016
Calderini DF, Castillo FM, Arenas-M A, Molero G, Reynolds MP, Craze M, Bowden S, Milner MJ, Wallington EJ, Dowle A, Gomez LD, McQueen-Mason SJ (2020) Overcoming the trade-off between grain weight and number in wheat by the ectopic expression of expansin in developing seeds leads to increased yield potential. New Phytol 230:629–640
Carra A, Gambino G, Schubert A (2007) A cetyltrimethylammonium bromide-based method to extract low-molecular-weight RNA from polysaccharide-rich plant tissues. Anal Biochem 360:318–320
Chen Q, Armstrong K (1994) Genomic in situ hybridization in Avena sativa. Genome 37:607–612
Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:884–890
Duan J, Wu Y, Zhou Y, Ren X, Shao Y, Feng W, Zhu Y, Wang Y, Guo T (2018) Grain number responses to pre-anthesis dry matter and nitrogen in improving wheat yield in the Huang-Huai Plain. Sci Rep 8:7126
Farashi A, Karimian Z (2021) Assessing climate change risks to the geographical distribution of grass species. Plant Signal Behav 16:e1913311
Glenn P, Woods DP, Zhang J, Gabay G, Odle N, Dubcovsky J (2023) Wheat bZIPC1 interacts with FT2 and contributes to the regulation of spikelet number per spike. Theor Appl Genet 136:237
Guo X, Shi Q, Liu Y, Su H, Zhang J, Wang M, Wang C, Wang J, Zhang K, Fu S, Hu X, Jing D, Wang Z, Li J, Zhang P, Liu C, Han F (2023) Systemic development of wheat–Thinopyrum elongatum translocation lines and their deployment in wheat breeding for Fusarium head blight resistance. Plant J 114:1475–1489
Gustavsson EK, Zhang D, Reynolds RH, Garcia-Ruiz S, Ryten M, Mathelier A (2022) ggtranscript: an R package for the visualization and interpretation of transcript isoforms using ggplot2. Bioinformatics 38:3844–3846
Hackauf B, Siekmann D, Fromme FJ (2022) Improving yield and yield stability in winter rye by hybrid breeding. Plants 11:2666
Han F, Gao Z, Birchler JA (2009) Reactivation of an inactive centromere reveals epigenetic and structural components for centromere specification in maize. Plant Cell 21:1929–1939
Han F, Lamb JC, Birchler JA (2006) High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize. Proc Natl Acad Sci 103:3238–3243
Han G, Liu S, Wang J, Jin Y, Zhou Y, Luo Q, Liu H, Zhao H, An D (2020) Identification of an elite wheat-rye T1RS·1BL translocation line conferring high resistance to powdery mildew and stripe rust. Plant Dis 104:2940–2948
Han H, Liu W, Lu Y, Zhang J, Yang X, Li X, Hu Z, Li L (2016) Isolation and application of P genome-specific DNA sequences of Agropyron Gaertn. in Triticeae. Planta 245:425–437
He H, Zhu S, Zhao R, Jiang Z, Ji Y, Ji J, Qiu D, Li H, Bie T (2018) Pm21, encoding a typical CC-NBS-LRR protein, confers broad-spectrum resistance to wheat powdery mildew disease. Mol Plant 11:879–882
Houtgast EJ, Sima V-M, Bertels K, Al-Ars Z (2018) Hardware acceleration of BWA-MEM genomic short read mapping for longer read lengths. Comput Biol Chem 75:54–64
Jiang B, Liu T, Li H, Han H, Li L, Zhang J, Yang X, Zhou S, Li X, Liu W (2018) Physical mapping of a novel locus conferring leaf rust resistance on the long arm of Agropyron cristatum chromosome 2P. Front Plant Sci 9:817
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL (2019) Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol 37:907–915
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Li H, Jiang B, Wang J, Lu Y, Zhang J, Pan C, Yang X, Li X, Liu W, Li L (2016) Mapping of novel powdery mildew resistance gene(s) from Agropyron cristatum chromosome 2P. Theor Appl Genet 130:109–121
Li L, Yang X, Li X, Dong Y, Chen X (1998) Introduction of desirable genes from Agropyron cristatum into common wheat by intergeneric hybridization. Sci Agricult Sin 31:1–6
Li T, Deng G, Tang Y, Su Y, Wang J, Cheng J, Yang Z, Qiu X, Pu X, Zhang H, Liang J, Yu M, Wei Y, Long H (2021) Identification and validation of a novel locus controlling spikelet number in bread wheat (Triticum aestivum L.). Front Plant Sci 12:611106
Li Z, Li B, Tong Y (2008) The contribution of distant hybridization with decaploid Agropyron elongatum to wheat improvement in China. J Genet Genom 35:451–456
Lin Y, Zhou S, Liang X, Guo B, Han B, Han H, Zhang J, Lu Y, Zhang Z, Yang X, Li X, Liu W, Li L (2022) Chromosomal mapping of a locus associated with adult-stage resistance to powdery mildew from Agropyron cristatum chromosome 6PL in wheat. Theor Appl Genet 135:2861–2873
Lin Y, Zhou S, Liang X, Han B, Yang J, Guo B, Zhang J, Han H, Liu W, Yang X, Li X, Li L (2023) Introgression of chromosome 6PL terminal segment from Agropyron cristatum to increase both grain number and grain weight in wheat. Crop J 11:878–886
Liu L, Luo Q, Li H, Li B, Li Z, Zheng Q (2018) Physical mapping of the blue-grained gene from Thinopyrum ponticum chromosome 4Ag and development of blue-grain-related molecular markers and a FISH probe based on SLAF-seq technology. Theor Appl Genet 131:2359–2370
Ma P, Han G, Zheng Q, Liu S, Han F, Wang J, Luo Q, An D (2020) Development of novel wheat–rye chromosome 4R translocations and assignment of their powdery mildew resistance. Plant Dis 104:260–268
Mago R, Miah H, Lawrence GJ, Wellings CR, Spielmeyer W, Bariana HS, McIntosh RA, Pryor AJ, Ellis JG (2005) High-resolution mapping and mutation analysis separate the rust resistance genes Sr31, Lr26 and Yr9 on the short arm of rye chromosome 1. Theor Appl Genet 112:41–50
Mater Y, Baenziger S, Gill K, Graybosch R, Whitcher L, Baker C, Specht J, Dweikat I (2004) Linkage mapping of powdery mildew and greenbug resistance genes on recombinant 1RS from ‘Amigo’ and ‘Kavkaz’ wheat–rye translocations of chromosome 1RS.1AL. Genome 47:292–298
Miransari M, Smith D (2019) Sustainable wheat (Triticum aestivum L.) production in saline fields: a review. Crit Rev Biotechnol 39:999–1014
Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842
Sakuma S, Golan G, Guo Z, Ogawa T, Tagiri A, Sugimoto K, Bernhardt N, Brassac J, Mascher M, Hensel G, Ohnishi S, Jinno H, Yamashita Y, Ayalon I, Peleg Z, Schnurbusch T, Komatsuda T (2019) Unleashing floret fertility in wheat through the mutation of a homeobox gene. Proc Natl Acad Sci 116:5182–5187
Schneider A, Rakszegi M, Molnár-Láng M, Szakács É (2016) Production and cytomolecular identification of new wheat-perennial rye (Secale cereanum) disomic addition lines with yellow rust resistance (6R) and increased arabinoxylan and protein content (1R, 4R, 6R). Theor Appl Genet 129:1045–1059
Song L, Jiang L, Han H, Gao A, Yang X, Li L, Liu W (2013) Efficient induction of Wheat-Agropyron cristatum 6P translocation lines and GISH detection. PLoS ONE 8:e69501
Song L, Lu Y, Zhang J, Pan C, Yang X, Li X, Liu W, Li L (2016a) Physical mapping of Agropyron cristatum chromosome 6P using deletion lines in common wheat background. Theor Appl Genet 129:1023–1034
Song L, Lu Y, Zhang J, Pan C, Yang X, Li X, Liu W, Li L (2016b) Cytological and molecular analysis of wheat–Agropyron cristatum translocation lines with 6P chromosome fragments conferring superior agronomic traits in common wheat. Genome 59:840–850
Tang Z, Yang Z, Fu S (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318
Wu J, Yang X, Wang H, Li H, Li L, Li X, Liu W (2006) The introgression of chromosome 6P specifying for increased numbers of florets and kernels from Agropyron cristatum into wheat. Theor Appl Genet 114:13–20
Xiao J, Liu B, Yao Y, Guo Z, Jia H, Kong L, Zhang A, Ma W, Ni Z, Xu S, Lu F, Jiao Y, Yang W, Lin X, Sun S, Lu Z, Gao L, Zhao G, Cao S, Chen Q, Zhang K, Wang M, Wang M, Hu Z, Guo W, Li G, Ma X, Li J, Han F, Fu X, Ma Z, Wang D, Zhang X, Ling H-Q, Xia G, Tong Y, Liu Z, He Z, Jia J, Chong K (2022) Wheat genomic study for genetic improvement of traits in China. Sci China Life Sci 65:1718–1775
Xing L, Hu P, Liu J, Witek K, Zhou S, Xu J, Zhou W, Gao L, Huang Z, Zhang R, Wang X, Chen P, Wang H, Jones JDG, Karafiátová M, Vrána J, Bartoš J, Doležel J, Tian Y, Wu Y, Cao A (2018) Pm21 from Haynaldia villosa encodes a CC-NBS-LRR protein conferring powdery mildew resistance in Wheat. Mol Plant 11:874–878
Yang G, Boshoff WHP, Li H, Pretorius ZA, Luo Q, Li B, Li Z, Zheng Q (2021a) Chromosomal composition analysis and molecular marker development for the novel Ug99-resistant wheat–Thinopyrum ponticum translocation line WTT34. Theor Appl Genet 134:1587–1599
Yang G, Deng P, Ji W, Fu S, Li H, Li B, Li Z, Zheng Q (2023) Physical mapping of a new powdery mildew resistance locus from Thinopyrum ponticum chromosome 4AgS. Front Plant Sci 14:1131205
Yang G, Tong C, Li H, Li B, Li Z, Zheng Q (2022) Cytogenetic identification and molecular marker development of a novel wheat–Thinopyrum ponticum translocation line with powdery mildew resistance. Theor Appl Genet 135:2041–2057
Yang G, Zheng Q, Hu P, Li H, Luo Q, Li B, Li Z (2021b) Cytogenetic identification and molecular marker development for the novel stripe rust-resistant wheat–Thinopyrum intermedium translocation line WTT11. aBIOTECH 2:343–356
Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134
Zhang X, Jia H, Li T, Wu J, Nagarajan R, Lei L, Powers C, Kan CC, Hua W, Liu Z, Chen C, Carver BF, Yan L (2022) TaCol-B5 modifies spike architecture and enhances grain yield in wheat. Science 376:180–183
Zhang Y, Zhang J, Huang L, Gao A, Zhang J, Yang X, Liu W, Li X, Li L (2015) A high-density genetic map for P genome of Agropyron Gaertn. Based on specific-locus amplified fragment sequencing (SLAF-seq). Planta 242:1335–1347
Zhang Z, Han H, Liu W, Song L, Zhang J, Zhou S, Yang X, Li X, Li L (2019) Deletion mapping and verification of an enhanced-grain number per spike locus from the 6PL chromosome arm of Agropyron cristatum in common wheat. Theor Appl Genet 132:2815–2827
Funding
This work was financially supported by the National Key R&D Program of China (2021YFD1200600).
Author information
Authors and Affiliations
Contributions
LHL conceived the research. YDL performed the research. YDL and SHZ wrote the paper. WJY modified some pictures. BH, XZL and YXZ participated in part of the data collection and cytology work. JPZ, HMH, BJG, XMY, XQL and WHL participated in the preparation of the reagents and materials used in this study.
Corresponding author
Ethics declarations
Conflict of interest
The authors have not disclosed any competing interests.
Additional information
Communicated by Peter Langridge.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lin, Y., Zhou, S., Yang, W. et al. Chromosomal mapping of a major genetic locus from Agropyron cristatum chromosome 6P that influences grain number and spikelet number in wheat. Theor Appl Genet 137, 82 (2024). https://doi.org/10.1007/s00122-024-04584-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00122-024-04584-2