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A promising QTL QSns.sau-MC-3D.1 likely superior to WAPO1 for the number of spikelets per spike of wheat shows no adverse effects on yield-related traits

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Abstract

Key message

A likely new locus QSns.sau-MC-3D.1 associated with SNS showing no negative effect on yield-related traits compared to WAPO1 was identified and validated in various genetic populations under multiple environments.

Abstract

The number of spikelets per spike (SNS) is one of the crucial factors determining wheat yield. Thus, improving our understanding of the genes that regulate SNS could help develop wheat varieties with higher yield. In this study, a recombinant inbred line (RIL) population (MC) containing 198 lines derived from a cross between msf and Chuannong 16 (CN16) was used to construct a genetic linkage map using the GenoBaits Wheat 16 K Panel. The genetic map contained 5,991 polymorphic SNP markers spanning 2,813.25 cM. A total of twelve QTL for SNS were detected, and two of them, i.e., QSns.sau-MC-3D.1 and QSns.sau-MC-7A, were stably expressed. QSns.sau-MC-3D.1 had high LOD values ranging from 4.99 to 11.06 and explained 9.71–16.75% of the phenotypic variation. Comparison of QSns.sau-MC-3D.1 with previously reported SNS QTL suggested that it is likely a novel one, and two kompetitive allele-specific PCR (KASP) markers were further developed. The positive effect of QSns.sau-MC-3D.1 was also validated in three biparental populations and a diverse panel containing 388 Chinese wheat accessions. Genetic analysis indicated that WHEAT ORTHOLOG OFAPO1 (WAPO1) was a candidate gene for QSns.sau-MC-7A. Pyramiding of QSns.sau-MC-3D.1 and WAP01 had a great additive effect increasing SNS by 7.10%. Correlation analysis suggested that QSns.sau-MC-3D.1 was likely independent of effective tiller number, plant height, spike length, anthesis date, and thousand kernel weight. However, the H2 haplotype of WAPO1 may affect effective tiller number and plant height. These results indicated that utilization of QSns.sau-MC-3D.1 should be given priority for wheat breeding. Geographical distribution analysis showed that the positive allele of QSns.nsau-MC-3D.1 was dominant in most wheat-producing regions of China, and it has been positively selected among modern cultivars released in China since the 1940s. Gene prediction, qRT-PCR analysis, and sequence alignment suggested that TraesCS3D03G0216800 may be the candidate gene of QSns.nsau-MC-3D.1. Taken together, these results enrich our understanding of the genetic basis of wheat SNS and will be useful for fine mapping and cloning of the gene underlying QSns.sau-MC-3D.1.

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files or from the corresponding authors upon reasonable request.

Abbreviations

AD:

Anthesis date

ANOVA:

Analysis of variance

BLUP:

Best linear unbiased prediction

CAW:

Chinese wheat accession

CMC:

Chinese modern cultivar

CS:

Chinese Spring

ETN:

Effective tiller number

IWGSC:

International Wheat Genome Sequencing Consortium

KASP:

Kompetitive allele-specific PCR

LY:

Luoyang

ML:

Mini-core collection

PH:

Plant height

PVE:

Phenotypic variance

QTL:

Quantitative trait loci

RIL:

Recombinant inbred line

SL:

Spike length

SNP:

Single nucleotide polymorphism

SNS:

The number of spikelets per spike

TKW:

Thousand kernel weight

WAPO1 :

WHEAT ORTHOLOG OFAPO1

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Acknowledgements

We thank Dr. Lihui Li (CAAS, China) for providing CAW accessions. We thank the anonymous referees for critical reading and revising this manuscript.

Funding

This work is supported by the Natural Science Foundation of Sichuan Province (2022NSFSC1729, 2023NSFSC0223), the Key Research and Development Program of Sichuan Province (2021YFYZ0002 and 2023YFSY0056), Sichuan Science and Technology Program (2022YFH0053 and 2021YFH0083), and Sichuan Province Science Foundation for Distinguished Young Scholars (2022JDJQ0006).

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Author notes

  1. Jieguang Zhou and Wei Li have contributed equally to this paper.

Authors and Affiliations

  1. State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China

    Jieguang Zhou, Wei Li, Yaoyao Yang, Xinlin Xie, Jiajun Liu, Yanling Liu, Huaping Tang, Mei Deng, Qiang Xu, Qiantao Jiang, Guoyue Chen, Pengfei Qi, Yunfeng Jiang, Youliang Zheng, Yuming Wei & Jian Ma

  2. Triticeae Research Institute, Sichuan Agricultural University, Chengdu, China

    Jieguang Zhou, Wei Li, Yaoyao Yang, Xinlin Xie, Jiajun Liu, Yanling Liu, Huaping Tang, Mei Deng, Qiang Xu, Qiantao Jiang, Guoyue Chen, Pengfei Qi, Yunfeng Jiang, Youliang Zheng, Yuming Wei & Jian Ma

  3. College of Resources, Sichuan Agricultural University, Chengdu, China

    Guangdeng Chen

  4. Mianyang Academy of Agricultural Science, Crop Characteristic Resources Creation and Utilization Key Laboratory of Sichuan Providence, Mianyang, China

    Yuanjiang He & Yong Ren

  5. Panzhihua Academy of Agricultural and Forestry Sciences, Panzhihua, China

    Liwei Tang

  6. College of Agronomy, Sichuan Agricultural University, Chengdu, China

    Lulu Gou

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  1. Jieguang Zhou
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Contributions

JGZ finished the study and wrote this manuscript. WL participated in field work and analyzed data. YYY, XLX, JJL, and MD helped phenotype measurement and data analysis. YLL, HPT, QX and QTJ did field work and data analysis. GYC, PFQ, YFJ, and GDC collected and analyzed data. YJH, YR, LWT, and LLG helped with data analysis. YLZ revised the manuscript. YMW discussed results and revised the manuscript. JM designed the experiments, guided the entire study, participated in data analysis, wrote, and extensively revised this manuscript. All authors participated in the research and approved the final manuscript.

Corresponding authors

Correspondence to Yuming Wei or Jian Ma.

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The authors have declared that no competing interests exist.

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All experiments and data analyses were conducted in Sichuan. All authors contributed to the study and approved the final version for submission. The manuscript has not been submitted to any other journal.

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Communicated by Takao Komatsuda.

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Supplementary Information

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122_2023_4429_MOESM1_ESM.tiff

Fig S1. Phenotypic distribution of SNS at five environments and BLUP. Red and black triangles represent the parents msf and CN16, respectively. (TIFF 896 kb)

122_2023_4429_MOESM2_ESM.tiff

Fig S2. Haplotype identification of WAPO1 in msf and CN16. (A), Promoter genotyping of WAPO1 in msf and CN16; (B), Genotyping of WAPO1 functional markers in msf and CN16. Blue boxes and orange round frames are the alleles with 140G and 140T, respectively. Black boxes are blank controls, and 20828 is the 140T positive control from a previous study (Ding et al. 2022). (TIFF 1252 kb)

122_2023_4429_MOESM3_ESM.tiff

Fig S3. Genetic map of the major QTL QSns.sau-MC-7A and the effect of WAPO1. (A), Genetic map of chromosome 3D containing the marker K-WAPO1. The pink area is the interval of QSns.sau-MC-7A. (B), A box plot that shows the effect of WAPO1 calculated after grouping the MC RIL population into two categories based on the K-WAPO1. Orange and gray boxes indicate lines are H2 and H3 haplotypes of WAPO1, respectively. **Significance level at P < 0.01. Differences in SNS between the lines of two haplotypes are labeled below the environment names and BLUP. (TIFF 655 kb)

122_2023_4429_MOESM4_ESM.tiff

Fig S4. Fluorescence PCR genotyping results of the KASP marker KASP-10 in four populations. (A-B), (C-E), (F-G), and (H-K), Fluorescence PCR genotyping results of the KASP marker KASP-10 in the four populations, msf × 3642, msf × 20828, msf × Shumai969, and CAW, respectively. Blue box (HEX fluorescence) represents lines with the homozygous genotype AA; The orange frame (FAM fluorescence) represents lines with the homozygous genotype GG; The green triangle represents lines with heterozygous genotype GA; Black boxes are blank controls. (TIFF 2301 kb)

122_2023_4429_MOESM5_ESM.tiff

Fig S5. Distribution of 143 Chinese landraces (A) and 245 modern cultivars (B) in ten production zones. I, northern winter wheat region; II, Yellow and Huai River valley winter wheat region; III, low and middle Yangtze River valley winter wheat region; IV, southwestern winter wheat region; V, southern winter wheat region; VI, northeastern spring wheat region; VII, northern spring wheat region; VIII, northwestern spring wheat region; IX, Qinghai–Tibet spring–winter wheat region; X, Xinjiang winter–spring wheat region. Student’s t-test comparing the values for SNS of two groups of accessions from the 143 Chinese landraces (C) and 245 modern cultivars (D) carrying the genotype either GG or AA for QSns.sau-MC-3D.1. *Significance level at P < 0.05, ns indicates no significant difference between the two groups. Percentage differences in SNS between the two groups are indicated above the P values. (TIFF 2173 kb)

122_2023_4429_MOESM6_ESM.tiff

Fig S6. Effect of 1BL/1RS translocations on SNS in the msf × CN16 population. The orange and gray box represents the lines with non-1BL/1RS translocations and 1BL/1RS translocations, respectively. ns indicates no significant difference between the two groups. Percentage differences in SNS between the two groups are indicated above the P values at the top of each plot. (TIFF 135 kb)

122_2023_4429_MOESM7_ESM.tiff

Fig S7. Expression pattern of genes within the QSns.sau-MC-3D.1 interval. A, Genes expressed in various tissues and their expression patterns; (B) and (C), the high-confidence 93 genes and their expression in six different developmental stages of spike, respectively. RV, LSV, LSS, LSR, SR, and GR represent root in vegetative stage, leaf or root in vegetative stage, leaf or root in seedling stage, leaf or root in reproductive stage, spike in reproductive stage, and grain in reproductive stage, respectively. KNI, KNII, KNIII, KNIV, KNV, and KNVI represent spikes in the vegetative stage, elongation stage, single ridge stage, double ridge stage, glume primordium differentiation stage, and floret differentiation stage, respectively. (TIFF 2259 kb)

122_2023_4429_MOESM8_ESM.tiff

Fig S8. Expression of TraesCS3D03G0222600 and TraesCS3D03G0216800 in the spike of parent msf and CN16. **Significance level at P < 0.01, and ns indicates no significant difference between the two groups. (TIFF 204 kb)

122_2023_4429_MOESM9_ESM.tiff

Fig S9. Comparison of QSns.sau-MC-3D.1 with previously reported SNS-related quantitative trait loci (QTL) and single nucleotide polymorphisms (SNPs). (A), Deletion bin map of wheat chromosome 3D; (B), Physical location ruler of wheat 3D chromosome; (C), Physical location of previously reported QTL/SNPs for SNS on the 3D chromosome. S, short arm; C, centromere; L, long arm. [a], (Zhai et al. 2016); [b], (Chen et al. 2017); [c], (Sun et al. 2017); [d], (Luo et al. 2016); [e], (Liu et al. 2006); [f], (Shukla et al. 2015). (TIFF 421 kb)

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Zhou, J., Li, W., Yang, Y. et al. A promising QTL QSns.sau-MC-3D.1 likely superior to WAPO1 for the number of spikelets per spike of wheat shows no adverse effects on yield-related traits. Theor Appl Genet 136, 181 (2023). https://doi.org/10.1007/s00122-023-04429-4

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