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Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Identification of quantitative trait loci underlying lodging of soybean across multiple environments

Maolin Sun A # , Kezhen Zhao A # , Jie Wang A , Wenqing Mu A , Yuhang Zhan A , Wenbin Li A , Weili Teng A , Xue Zhao https://orcid.org/0000-0003-3362-1471 A * and Yingpeng Han https://orcid.org/0000-0002-9829-6588 A *
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Soybean Biology in Chinese Ministry of Education (Key Laboratory of Soybean Biology and Breeding/Genetics of Chinese Agriculture Ministry), Northeast Agricultural University, 150030 Harbin, China.

# These authors contributed equally to this paper

Handling Editor: Marta Santalla

Crop & Pasture Science 73(6) 652-662 https://doi.org/10.1071/CP21468
Submitted: 29 June 2021  Accepted: 1 December 2021   Published: 21 March 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Lodging is an important agronomic trait related to crop yield and is easily susceptible to environmental influences. In this study, a recombinant inbred line population from soybean (Glycine max (L.) Merr.) Hefeng 25 × Dongnong L28 including 109 lines was used to identify quantitative trait loci (QTLs) related to soybean lodging. Seven QTLs were identified in the three environments (Harbin in 2017, 2018 and 2019), and these could explain 2.21–20.17% of the phenotypic variation. Among these QTLs, qLDG-I-1 (Chr20_24146101–Chr20_24297321) was stable for multiple environments. A residue heterozygous line, which was heterozygous at the qLDG-I-1 locus, was used to verify qLDG-I-1, and the results showed that this QTL could significantly improve lodging resistance of soybean. Meanwhile, 13 pairs of epistatic QTLs were detected, which could explain 3.26–18.24% of the phenotypic variation. QTL × environment interaction mapping was also used, and it detected 31 QTLs, which could explain 1.61–7.94% of the phenotypic variation. In total, 122 pairs of epistatic QTLs were detected, and they could explain 5.39–27.81% of the phenotypic variation. Additionally, candidate genes related to soybean lodging in the qLDG-I-1 interval were predicted, and Glyma.20g068000 was mined as a candidate gene based on quantitative real-time PCR analysis. The QTLs and candidate genes identified in this study are of great significance to position cloning, and could accelerate the progress of breeding resistance to lodging in soybean.

Keywords: candidate genes, crop yield, environment interaction, lodging, QTL, recombinant inbred line, SNP markers, soybean.


References

Abdel-Haleem H, Lee G-J, Boerma RH (2011) Identification of QTL for increased fibrous roots in soybean. Theoretical and Applied Genetics 122, 935–946.
Identification of QTL for increased fibrous roots in soybean.Crossref | GoogleScholarGoogle Scholar | 21165732PubMed |

Antwi-Boasiako A (2017) Screening of soybean (Glycine max (L.) Merrill) genotypes for resistance to lodging and pod shattering. International Journal of Agronomy and Agricultural Research (IJAAR) 10, 1–8.
Screening of soybean (Glycine max (L.) Merrill) genotypes for resistance to lodging and pod shattering.Crossref | GoogleScholarGoogle Scholar |

Chen H, Shan Z, Sha A, Wu B, Yang Z, Chen S, Zhou R, Zhou X (2011) Quantitative trait loci analysis of stem strength and related traits in soybean. Euphytica 179, 485–497.
Quantitative trait loci analysis of stem strength and related traits in soybean.Crossref | GoogleScholarGoogle Scholar |

Cornelious B, Chen P, Chen Y, de Leon N, Shannon JG, Wang D (2005) Identification of QTLs underlying water-logging tolerance in soybean. Molecular Breeding 16, 103–112.
Identification of QTLs underlying water-logging tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |

Fan D, Yang Z, Ma Z, Zeng Q, Jiang H, Liu C, Han D, Luan H, Pei Y, Chen Q (2012) QTL analysis of lodging-resistance related traits in soybean in different environments. Scientia Agricultura Sinica 45, 3029–3039.

Fan C, Li Y, Hu Z, Hu H, Wang G, Li A, Wang Y, Tu Y, Xia T, Peng L, Feng S (2018) Ectopic expression of a novel OsExtensin-like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice. Plant Biotechnology Journal 16, 254–263.
Ectopic expression of a novel OsExtensin-like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice.Crossref | GoogleScholarGoogle Scholar | 28574641PubMed |

Kang MS, Din AK, Zhang Y, Magari R (1999) Combining ability for rind puncture resistance in maize. Crop Science 39, 368–371.
Combining ability for rind puncture resistance in maize.Crossref | GoogleScholarGoogle Scholar |

Kashiwagi T, Ishimaru K (2004) Identification and functional analysis of a locus for improvement of lodging resistance in rice. Plant Physiology 134, 676–683.
Identification and functional analysis of a locus for improvement of lodging resistance in rice.Crossref | GoogleScholarGoogle Scholar | 14739343PubMed |

Kim HS, Diers BW (2000) Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Science 40, 55–61.
Inheritance of partial resistance to Sclerotinia stem rot in soybean.Crossref | GoogleScholarGoogle Scholar |

Kim K-S, Diers BW, Hyten DL, Rouf Mian MA, Shannon JG, Nelson RL (2012) Identification of positive yield QTL alleles from exotic soybean germplasm in two backcross populations. Theoretical and Applied Genetics 125, 1353–1369.
Identification of positive yield QTL alleles from exotic soybean germplasm in two backcross populations.Crossref | GoogleScholarGoogle Scholar | 22869284PubMed |

Lark KG, Chase K, Adler F, Mansur LM, Orf JH (1995) Interactions between quantitative trait loci in soybean in which trait variation at one locus is conditional upon a specific allele at another. Proceedings of the National Academy of Sciences of the United States of America 92, 4656–4660.
Interactions between quantitative trait loci in soybean in which trait variation at one locus is conditional upon a specific allele at another.Crossref | GoogleScholarGoogle Scholar | 7753859PubMed |

Lee SH, Bailey MA, Mian MAR, Carter TE, Ashley DA, Hussey RS, Parrott WA, Boerma HR (1996a) Molecular markers associated with soybean plant height, lodging, and maturity across locations. Crop Science 36, 728–735.
Molecular markers associated with soybean plant height, lodging, and maturity across locations.Crossref | GoogleScholarGoogle Scholar |

Lee SH, Bailey MA, Mian MAR, Shipe ER, Ashley DA, Parrott WA, Hussey RS, Boerma HR (1996b) Identification of quantitative trait loci for plant height, lodging, and maturity in a soybean population segregating for growth habit. Theoretical and Applied Genetics 92, 516–523.
Identification of quantitative trait loci for plant height, lodging, and maturity in a soybean population segregating for growth habit.Crossref | GoogleScholarGoogle Scholar | 24166318PubMed |

Lee S, Jun TH, Michel AP, Rouf Mian MA (2015) SNP markers linked to QTL conditioning plant height, lodging, and maturity in soybean. Euphytica 203, 521–532.
SNP markers linked to QTL conditioning plant height, lodging, and maturity in soybean.Crossref | GoogleScholarGoogle Scholar |

Li F, Xie G, Huang J, Zhang R, Li Y, Zhang M, Wang Y, Li A, Li X, Xia T, Qu C, Hu F, Ragauskas AJ, Peng L (2017) OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice. Plant Biotechnology Journal 15, 1093–1104.
OsCESA9 conserved-site mutation leads to largely enhanced plant lodging resistance and biomass enzymatic saccharification by reducing cellulose DP and crystallinity in rice.Crossref | GoogleScholarGoogle Scholar | 28117552PubMed |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lukens L, Doebley J (1999) Epistatic and environmental interactions for quantitative trait loci involved in maize evolution. Genetical Research 74, 291–302.
Epistatic and environmental interactions for quantitative trait loci involved in maize evolution.Crossref | GoogleScholarGoogle Scholar |

Mansur LM, Orf JH, Chase K, Jarvik T, Cregan PB, Lark KG (1996) Genetic mapping of agronomic traits using recombinant inbred lines of soybean. Crop Science 36, 1327–1336.
Genetic mapping of agronomic traits using recombinant inbred lines of soybean.Crossref | GoogleScholarGoogle Scholar |

Matsuo N, Yamada T, Takada Y, Fukami K, Hajika M (2018) Effect of plant density on growth and yield of new soybean genotypes grown under early planting condition in southwestern Japan. Plant Production Science 21, 16–25.
Effect of plant density on growth and yield of new soybean genotypes grown under early planting condition in southwestern Japan.Crossref | GoogleScholarGoogle Scholar |

McCouch SR, Cho YG, Yano M (1997) Report on QTL nomenclature. Rice Genetic Newsletter 14, 11–13.

Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. The Crop Journal 3, 269–283.
QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations.Crossref | GoogleScholarGoogle Scholar |

Oguchi T, Sage-Ono K, Kamada H, Ono M (2004) Genomic structure of a novel Arabidopsis clock-controlled gene, AtC401, which encodes a pentatricopeptide repeat protein. Gene 330, 29–37.
Genomic structure of a novel Arabidopsis clock-controlled gene, AtC401, which encodes a pentatricopeptide repeat protein.Crossref | GoogleScholarGoogle Scholar | 15087121PubMed |

Orf JH, Chase K, Jarvik T, Mansur LM, Cregan PB, Adler FR, Lark KG (1999) Genetics of soybean agronomic traits: I. Comparison of three related recombinant inbred populations. Crop Science 39, 1642–1651.
Genetics of soybean agronomic traits: I. Comparison of three related recombinant inbred populations.Crossref | GoogleScholarGoogle Scholar |

Pei R, Zhang J, Tian L, Zhang S, Han F, Yan S, Wang L, Li B, Sun J (2018) Identification of novel QTL associated with soybean isoflavone content. The Crop Journal 6, 244–252.
Identification of novel QTL associated with soybean isoflavone content.Crossref | GoogleScholarGoogle Scholar |

Reinprecht Y, Poysa VW, Yu K, Rajcan I, Ablett GR, Pauls KP (2006) Seed and agronomic QTL in low linolenic acid, lipoxygenase-free soybean (Glycine max (L.) Merrill) germplasm. Genome 49, 1510–1527.
Seed and agronomic QTL in low linolenic acid, lipoxygenase-free soybean (Glycine max (L.) Merrill) germplasm.Crossref | GoogleScholarGoogle Scholar | 17426766PubMed |

Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Séguin A (2005) CINNAMYL ALCOHOL DEHYDROGENASE-C and-D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. The Plant Cell 17, 2059–2076.
CINNAMYL ALCOHOL DEHYDROGENASE-C and-D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 15937231PubMed |

Specht JE, Chase K, Macrander M, Graef GL, Chung J, Markwell JP, Germann M, Orf JH, Lark KG (2001) Soybean response to water: a QTL analysis of drought tolerance. Crop Science 41, 493–509.
Soybean response to water: a QTL analysis of drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Sun M, Li N, Yu K, Zhan Y, Yuan M, Teng W, Li W, Zhao X, Xiao J, Han Y (2021) QTL mapping of lodging tolerance in soybean. Crop & Pasture Science 72, 426–433.
QTL mapping of lodging tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |

Sung M, Van K, Lee S, Nelson R, LaMantia J, Taliercio E, McHale LK, Mian MAR (2021) Identification of SNP markers associated with soybean fatty acids contents by genome-wide association analyses. Molecular Breeding 41, 27
Identification of SNP markers associated with soybean fatty acids contents by genome-wide association analyses.Crossref | GoogleScholarGoogle Scholar |

Uchikawa O, Miyazaki M, Tanaka K (2006) The relationship lodging of soybean and the combine harvesting loss in Fukuoka Prefecture in 2004. Report of the Kyushu Branch of the Crop Science Society of Japan 72, 32–34.

Woods SJ, Swearingin ML (1977) Influence of simulated early lodging upon soybean seed yield and its components. Agronomy Journal 69, 239–242.
Influence of simulated early lodging upon soybean seed yield and its components.Crossref | GoogleScholarGoogle Scholar |

Wu J, Yan M, Zhang D, Zhou D, Yamaguchi N, Ito T (2020) Histone demethylases coordinate the antagonistic interaction between abscisic acid and brassinosteroid signaling in Arabidopsis. Frontiers in Plant Science 11, 596835
Histone demethylases coordinate the antagonistic interaction between abscisic acid and brassinosteroid signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 33324437PubMed |

Xing W, Zhao H, Zou D (2014) Detection of main-effect and epistatic QTL for yield-related traits in rice under drought stress and normal conditions. Canadian Journal of Plant Science 94, 633–641.
Detection of main-effect and epistatic QTL for yield-related traits in rice under drought stress and normal conditions.Crossref | GoogleScholarGoogle Scholar |

Yadav S, Singh UM, Naik SM, Venkateshwarlu C, Ramayya PJ, Raman KA, Sandhu N, Kumar A (2017) Molecular mapping of QTLs associated with lodging resistance in dry direct-seeded rice (Oryza sativa L.). Frontiers in Plant Science 8, 1431
Molecular mapping of QTLs associated with lodging resistance in dry direct-seeded rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 28871266PubMed |

Yamaguchi N, Sayama T, Yamazaki H, Miyoshi T, Ishimoto M, Funatsuki H (2014) Quantitative trait loci associated with lodging tolerance in soybean cultivar ‘Toyoharuka’. Breeding Science 64, 300–308.
Quantitative trait loci associated with lodging tolerance in soybean cultivar ‘Toyoharuka’.Crossref | GoogleScholarGoogle Scholar | 25914584PubMed |

Zhang B, Deng L, Qian Q, Xiong G, Zeng D, Li R, Guo L, Li J, Zhou Y (2009) A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice. Plant Molecular Biology 71, 509
A missense mutation in the transmembrane domain of CESA4 affects protein abundance in the plasma membrane and results in abnormal cell wall biosynthesis in rice.Crossref | GoogleScholarGoogle Scholar | 19697141PubMed |

Zhang Y, Liu P, Zhang X, Zheng Q, Chen M, Ge F, Li Z, Sun W, Guan Z, Liang T, Zheng Y, Tan X, Zou C, Peng H, Pan G, Shen Y (2018) Multi-locus genome-wide association study reveals the genetic architecture of stalk lodging resistance-related traits in maize. Frontiers in Plant Science 9, 611
Multi-locus genome-wide association study reveals the genetic architecture of stalk lodging resistance-related traits in maize.Crossref | GoogleScholarGoogle Scholar | 29868068PubMed |

Zhao X, Bao D, Wang W, Zhang C, Jing Y, Jiang H, Qiu L, Li W, Han Y (2020) Loci and candidate gene identification for soybean resistance to Phytophthora root rot race 1 in combination with association and linkage mapping. Molecular Breeding 40, 100
Loci and candidate gene identification for soybean resistance to Phytophthora root rot race 1 in combination with association and linkage mapping.Crossref | GoogleScholarGoogle Scholar |