Abstract
Main conclusion
Four heterotic QTL and a heterozygous segment for plant weight were identified by Graded Pool-Seq, QTL-seq and traditional genetic linkage analysis in heading Chinese cabbage.
Abstract
Heading Chinese cabbage (Brassica rapa L. spp. pekinensis) is a cross-pollinated leafy vegetable with significant heterosis. The use of heterosis is important for breeding high-yield Chinese cabbage hybrids. However, the formation and mechanism of heterosis have not been studied. We dissected the molecular mechanism of heterosis of yield-related traits in Chinese cabbage. An F1 hybrid with high-parent heterosis of yield-related traits was selected and self-pollinated to generate segregating F2 populations. QTL-seq, Graded Pool-seq (GPS), and traditional genetic linkage analysis were used to identify four heterotic quantitative trait loci (QTL) for plant weight: qPW1.1, qPW5.1, qPW7.1, and qPW8.1. Traditional genetic linkage analysis over two years showed that qPW8.1, located in marker A08_S45 (18,172,719) and A08_S85 (18,196,752), was mapped to a 23.5 kb genomic region. QTL qPW8.1 explained 8.6% and 23.6% of the phenotypic variation in plant weight and the total numbers of head leaves, respectively, and contained a heterozygous segment that might control the heterosis of plant weight. The qPW1.1 made an 11.7% phenotypic contribution to plant weight. The qPW7.1 was sensitive to environmental influence and explained 10.7% of the phenotypic variance. QTL qPW5.1 had a significant signal and was located in a genetic region near the centromere showing high heterozygosity. The “pseudo-overdominance” and “synergistic allelic” effects from parent line “XJD4” appear to play an important role in heterosis for plant weight in Chinese cabbage. These results provide a basis for an improved understanding of the molecular mechanism of yield-related traits and their heterosis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in the supplementary information files.
Abbreviations
- ED:
-
Euclidean distance
- GPS:
-
Graded Pool-Seq
- HHE:
-
Honghaier
- LOD:
-
Logarithm of the odds
- QTL:
-
Quantitative trait loci
- SNP:
-
Single nucleotide polymorphism
- XJD4:
-
XinJingdian 4
References
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30(2):174–178. https://doi.org/10.1038/nbt.2095
Birchler JA, Veitia RA (2010) The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol 186(1):54–62. https://doi.org/10.1111/j.1469-8137.2009.03087.x
Bruce AB (1910) The Mendelian theory of heredity and the augmentation of vigor. Science 32(827):627–628. https://doi.org/10.1126/science.32.827.627-a
Cai X, Wu J, Liang J, Lin R, Zhang K, Cheng F, Wang X (2020) Improved Brassica oleracea JZS assembly reveals significant changing of LTR-RT dynamics in different morphotypes. Theor Appl Genet 133(11):3187–3199. https://doi.org/10.1007/s00122-020-03664-3
Cingolani P, Platts A, le Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (austin) 6(2):80–92. https://doi.org/10.4161/fly.19695
Das S, Upadhyaya HD, Bajaj D, Kujur A, Badoni S, Laxmi KV, Tripathi S, Gowda CL, Sharma S, Singh S, Tyagi AK, Parida SK (2015) Deploying QTL-seq for rapid delineation of a potential candidate gene underlying major trait-associated QTL in chickpea. DNA Res 22(3):193–203. https://doi.org/10.1093/dnares/dsv004
Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28(718):454–455. https://doi.org/10.1126/science.28.718.454-b
Fu D, Xiao M, Hayward A, Jiang G, Zhu L, Zhou Q, Li J, Zhang M (2015) What is crop heterosis: new insights into an old topic. J Appl Genet 56(1):1–13. https://doi.org/10.1007/s13353-014-0231-z
Hill JT, Demarest BL, Bisgrove BW, Gorsi B, Su YC, Yost HJ (2013) MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res 23(4):687–697. https://doi.org/10.1101/gr.146936.112
Hochholdinger F, Baldauf JA (2018) Heterosis in plants. Curr Biol 28(18):R1089–R1092. https://doi.org/10.1016/j.cub.2018.06.041
Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Lu Y, Weng Q, Han B (2016a) Genomic architecture of heterosis for yield traits in rice. Nature 537(7622):629–633. https://doi.org/10.1038/nature19760
Huang YJ, Jestin C, Welham SJ, King GJ, Manzanares-Dauleux MJ, Fitt BD, Delourme R (2016b) Identification of environmentally stable QTL for resistance against Leptosphaeria maculans in oilseed rape (Brassica napus). Theor Appl Genet 129(1):169–180. https://doi.org/10.1007/s00122-015-2620-z
Huang YJ, Paillard S, Kumar V, King GJ, Fitt BDL, Delourme R (2019) Oilseed rape (Brassica napus) resistance to growth of Leptosphaeria maculans in leaves of young plants contributes to quantitative resistance in stems of adult plants. PLoS ONE 14(9):e0222540. https://doi.org/10.1371/journal.pone.0222540
Illa-Berenguer E, Van Houten J, Huang Z, van der Knaap E (2015) Rapid and reliable identification of tomato fruit weight and locule number loci by QTL-seq. Theor Appl Genet 128(7):1329–1342. https://doi.org/10.1007/s00122-015-2509-x
Ishii T, Juranić M, Maheshwari S, Bustamante FO, Vogt M, Salinas-Gamboa R, Dreissig S, Gursanscky N, How T, Demidov D, Fuchs J, Schubert V, Spriggs A, Vielle-Calzada JP, Comai L, Koltunow AMG, Houben A (2020) Unequal contribution of two paralogous CENH3 variants in cowpea centromere function. Commun Biol 3(1):775. https://doi.org/10.1038/s42003-020-01507-x
Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2(5):466–479
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x
Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42(5):459
Kumar V, Paillard S, Fopa-Fomeju B, Falentin C, Deniot G, Baron C, Vallée P, Manzanares-Dauleux MJ, Delourme R (2018) Multi-year linkage and association mapping confirm the high number of genomic regions involved in oilseed rape quantitative resistance to blackleg. Theor Appl Genet 131(8):1627–1643. https://doi.org/10.1007/s00122-018-3103-9
Larièpe A, Mangin B, Jasson S, Combes V, Dumas F, Jamin P, Lariagon C, Jolivot D, Madur D, Fiévet J, Gallais A, Dubreuil P, Charcosset A, Moreau L (2012) The genetic basis of heterosis: multiparental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.). Genetics 190(2):795–811. https://doi.org/10.1534/genetics.111.133447
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li D, Huang Z, Song S, Xin Y, Mao D, Lv Q, Zhou M, Tian D, Tang M, Wu Q, Liu X, Chen T, Song X, Fu X, Zhao B, Liang C, Li A, Liu G, Li S, Hu S, Cao X, Yu J, Yuan L, Chen C, Zhu L (2016) Integrated analysis of phenome, genome, and transcriptome of hybrid rice uncovered multiple heterosis-related loci for yield increase. Proc Natl Acad Sci USA 113(41):E6026-e6035. https://doi.org/10.1073/pnas.1610115113
Li P, Su T, Zhang D, Wang W, Xin X, Yu Y, Zhao X, Yu S, Zhang F (2021) Genome-wide analysis of changes in miRNA and target gene expression reveals key roles in heterosis for Chinese cabbage biomass. Hortic Res 8(1):39. https://doi.org/10.1038/s41438-021-00474-6
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Liu J, Li M, Zhang Q, Wei X, Huang X (2020) Exploring the molecular basis of heterosis for plant breeding. J Integr Plant Biol 62(3):287–298. https://doi.org/10.1111/jipb.12804
Lu H, Lin T, Klein J, Wang S, Qi J, Zhou Q, Sun J, Zhang Z, Weng Y, Huang S (2014) QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber. Theor Appl Genet 127(7):1491–1499. https://doi.org/10.1007/s00122-014-2313-z
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303. https://doi.org/10.1101/gr.107524.110
McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, Brown P, Browne C, Eller M, Guill K, Harjes C, Kroon D, Lepak N, Mitchell SE, Peterson B, Pressoir G, Romero S, Oropeza Rosas M, Salvo S, Yates H, Hanson M, Jones E, Smith S, Glaubitz JC, Goodman M, Ware D, Holland JB, Buckler ES (2009) Genetic properties of the maize nested association mapping population. Science 325(5941):737–740. https://doi.org/10.1126/science.1174320
Ooijen JWv, Voorrips RE (2001)Software for the calculation of genetic linkage maps.
Ooijen JV, Ooijen JV, Ooijen J, Hoorn J, Duin J, Van JW (2009) MapQTL®6. Software for the mapping of quantitative trait loci in experimental populations of diploid species.
Saeki N, Kawanabe T, Ying H, Shimizu M, Kojima M, Abe H, Okazaki K, Kaji M, Taylor JM, Sakakibara H, Peacock WJ, Dennis ES, Fujimoto R (2016) Molecular and cellular characteristics of hybrid vigour in a commercial hybrid of Chinese cabbage. BMC Plant Biol 16:45. https://doi.org/10.1186/s12870-016-0734-3
Schnell FW, Cockerham CC (1992) Multiplicative vs arbitrary gene action in heterosis. Genetics 131(2):461–469
Shu J, Liu Y, Zhang L, Li Z, Fang Z, Yang L, Zhuang M, Zhang Y, Lv H (2018) QTL-seq for rapid identification of candidate genes for flowering time in broccoli x cabbage. Theor Appl Genet 131(4):917–928. https://doi.org/10.1007/s00122-017-3047-5
Shull GH (1948) What is heterosis? Genetics 33(5):439
Singh VK, Khan AW, Jaganathan D, Thudi M, Roorkiwal M, Takagi H, Garg V, Kumar V, Chitikineni A, Gaur PM, Sutton T, Terauchi R, Varshney RK (2016a) QTL-seq for rapid identification of candidate genes for 100-seed weight and root/total plant dry weight ratio under rainfed conditions in chickpea. Plant Biotechnol J 14(11):2110–2119. https://doi.org/10.1111/pbi.12567
Singh VK, Khan AW, Saxena RK, Kumar V, Kale SM, Sinha P, Chitikineni A, Pazhamala LT, Garg V, Sharma M, Sameer Kumar CV, Parupalli S, Vechalapu S, Patil S, Muniswamy S, Ghanta A, Yamini KN, Dharmaraj PS, Varshney RK (2016b) Next-generation sequencing for identification of candidate genes for Fusarium wilt and sterility mosaic disease in pigeonpea (Cajanus cajan). Plant Biotechnol J 14(5):1183–1194. https://doi.org/10.1111/pbi.12470
Su T, Li P, Yang J, Sui G, Yu Y, Zhang D, Zhao X, Wang W, Wen C, Yu S, Zhang F (2018) Development of cost-effective single nucleotide polymorphism marker assays for genetic diversity analysis in Brassica rapa. Mol Breed. https://doi.org/10.1007/s11032-018-0795-0
Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74(1):174–183. https://doi.org/10.1111/tpj.12105
Wang X, Wu J, Liang J, Cheng F, Wang X (2015) Brassica database (BRAD) version 20: integrating and mining Brassicaceae species genomic resources. Database (oxford). https://doi.org/10.1093/database/bav093
Wang Y, Zhang X, Shi X, Sun C, Jin J, Tian R, Wei X, Xie H, Guo Z, Tang J (2018) Heterotic loci identified for maize kernel traits in two chromosome segment substitution line test populations. Sci Rep 8(1):11101. https://doi.org/10.1038/s41598-018-29338-1
Wang C, Tang S, Zhan Q, Hou Q, Zhao Y, Zhao Q, Feng Q, Zhou C, Lyu D, Cui L, Li Y, Miao J, Zhu C, Lu Y, Wang Y, Wang Z, Zhu J, Shangguan Y, Gong J, Yang S, Wang W, Zhang J, Xie H, Huang X, Han B (2019) Dissecting a heterotic gene through GradedPool-Seq mapping informs a rice-improvement strategy. Nat Commun 10(1):2982. https://doi.org/10.1038/s41467-019-11017-y
Wu J, Sun D, Zhao Q, Yong H, Zhang D, Hao Z, Zhou Z, Han J, Zhang X, Xu Z, Li X, Li M, Weng J (2021a) Transcriptome reveals allele contribution to heterosis in maize. Front Plant Sci 12:2143. https://doi.org/10.3389/fpls.2021a.739072
Wu X, Liu Y, Zhang Y, Gu R (2021b) Advances in research on the mechanism of heterosis in plants. Front Plant Sci 12:745726. https://doi.org/10.3389/fpls.2021.745726
Yue L, Li G, Zhang S, Zhang S, Zhang H, Li F, Sun R (2021) Interesting finding: The centromere sequences of doubled haploid (DH) were heterozygous in Brassica rapa L. Biomed J Sci Tech Res 33(2):25613–25615. https://doi.org/10.26717/bjstr.2021.33.005365
Zhang L, Cai X, Wu J, Liu M, Grob S, Cheng F, Liang J, Cai C, Liu Z, Liu B, Wang F, Li S, Liu F, Li X, Cheng L, Yang W, Li MH, Grossniklaus U, Zheng H, Wang X (2018) Improved Brassica rapa reference genome by single-molecule sequencing and chromosome conformation capture technologies. Hortic Res 5:50. https://doi.org/10.1038/s41438-018-0071-9
Zhou X, Huang X (2019) Genome-wide association studies in rice: how to solve the low power problems? Mol Plant 12(1):10–12. https://doi.org/10.1016/j.molp.2018.11.010
Zhu YJ, Huang DR, Fan YY, Zhang ZH, Ying JZ, Zhuang JY (2016) Detection of QTLs for yield heterosis in rice using a RIL population and its testcross population. Int J Genomics 2016:2587823. https://doi.org/10.1155/2016/2587823
Zou C, Wang P, Xu Y (2016) Bulked sample analysis in genetics, genomics and crop improvement. Plant Biotechnol J 14(10):1941–1955. https://doi.org/10.1111/pbi.12559
Acknowledgements
We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Funding
This work was funded by the National Key Research and Development Program of China (Grant number 2016YFD0101701), the China Agricultural Research System (CARS-23-A14), and Central Public-interest Scientific Institution Basal Research Fund (No. IVF-BRF2020004). This work was performed at the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, Beijing, China.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare that they have no competing interests.
Additional information
Communicated by Dorothea Bartels.
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
About this article
Cite this article
Yue, L., Sun, R., Li, G. et al. Genetic dissection of heterotic loci associated with plant weight by Graded pool-seq in heading Chinese cabbage (Brassica rapa). Planta 255, 126 (2022). https://doi.org/10.1007/s00425-022-03880-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-022-03880-9