Mining candidate genes associated with growth traits in Schima superba using eQTL and WGCNA

LU Yaojia, YULUO Zhuoma, CHENG Yuhang, WANG Yunpeng, TANG Xinghao, SHAO Wen, ZHOU Zhichun, ZHANG Rui

Journal of Nanjing Forestry University (Natural Sciences Edition) ›› 0

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Journal of Nanjing Forestry University (Natural Sciences Edition) ›› 0 DOI: 10.12302/j.issn.1000-2006.202604021

Mining candidate genes associated with growth traits in Schima superba using eQTL and WGCNA

  • LU Yaojia1,2, YULUO Zhuoma1, CHENG Yuhang1, WANG Yunpeng3, TANG Xinghao4, SHAO Wen5, ZHOU Zhichun1, ZHANG Rui1,*
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Abstract

【Objective】The formation of tree height and diameter at breast height in Schima superba is regulated by complex molecular networks. This study aimed to identify the genes and loci associated with these growth traits, thereby providing precise targets for the breeding of fast-growing trees. 【Method】A total of 186 individuals representing 24 provenances from 18-year-old S. superba plantations were used in this study. Phenotypic traits, including tree height and diameter at breast height, were measured, and cambium and secondary xylem tissues were collected for transcriptome sequencing. Weighted gene co-expression network analysis (WGCNA) and expression quantitative trait locus (eQTL) mapping were combined to identify genetic loci and candidate genes significantly associated with tree height and diameter at breast height, and to further clarify their regulatory networks. 【Result】A total of 30 786 eQTLs were identified at the whole-genome level, regulating the expression of 7 224 genes. Compared with distant eQTLs, local eQTLs showed higher significance and explained a greater proportion of the variation in gene expression. WGCNA identified 16 co-expression modules. Among them, the black module was significantly positively correlated with both tree height and diameter at breast height (r = 0.47 and 0.43, p < 0.01), while the green module was significantly negatively correlated with these traits (r = -0.51 and -0.46, p < 0.01). Integrative analysis of WGCNA and eQTL revealed that Ssu10G00379 (SsuMYB152), a MYB3R transcription factor, was associated with both a local eQTL (SNP_chr10_4859354) and a distant eQTL interval, indicating that it is an important regulatory node linking genetic variation to tree height. Higher expression of this gene was significantly associated with the A genotype at SNP_chr10_4859354 (p = 9.64 × 10-9) and was extremely significantly positively correlated with higher tree height (r = 0.40, p < 1.2 × 10-8). Taking SsuMYB152 as the core gene, 87 candidate genes significantly associated with microtubule movement, cell morphogenesis, plant hormone signaling and MAPK signaling pathway were identified (r > 0.6, FDR < 0.01). The interaction network showed that SsuMYB152 was closely connected with several genes involved in cell cycle and growth development, including CYCB1-2, CYCB2-4, CDKB1-2, UBC20, KIN12B, KIN13B, and TAN. 【Conclusion】The A genotype of the local eQTL locus SNP_chr10_4859354 was associated with higher expression of SsuMYB152, and the higher expression of this gene was significantly correlated with increased tree height (r = 0.40, p < 1.2 × 10-8). This gene was also affected by a distant eQTL and served as a key regulatory node linking genetic variation to tree height.

Key words

Schima superba / MYB / eQTLs / WGCNA / tree height / genetic improvement

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LU Yaojia, YULUO Zhuoma, CHENG Yuhang, WANG Yunpeng, TANG Xinghao, SHAO Wen, ZHOU Zhichun, ZHANG Rui. Mining candidate genes associated with growth traits in Schima superba using eQTL and WGCNA[J]. Journal of Nanjing Forestry University (Natural Sciences Edition). 0 https://doi.org/10.12302/j.issn.1000-2006.202604021

References

[1] 赵奋成, 郭文冰, 林昌明, 等. 湿地松自由授粉家系松脂产量性状和生长性状的遗传变异分析[J]. 华南农业大学学报, 2020, 41(4): 90-94. DOI:10.7671/j.issn.1001-411X.201911002.
ZHAO F C, GUO W B, LIN C M, et al.Genetic variation analysis on oleoresin yield and growth traits of Pinus elliottii open-pollinated families[J]. Journal of South China Agricultural University, 2020, 41(4): 90-94. DOI:10.7671/j.issn.1001-411X.201911002.
[2] LI Y, SUONTAMA M, BURDON R D, et al.Genotype by environment interactions in forest tree breeding: review of methodology and perspectives on research and application[J]. Tree Genetics & Genomes, 2017, 13(3): 60. DOI:10.1007/s11295-017-1144-x.
[3] LENZ P R N, BEAULIEU J, MANSFIELD S D, et al. Factors affecting the accuracy of genomic selection for growth and wood quality traits in an advanced-breeding population of black spruce (Picea mariana)[J]. BMC Genomics, 2017, 18: 335. DOI:10.1186/s12864-017-3715-5.
[4] PARVEEN R, KUMAR M, SWAPNIL, et al. Understanding the genomic selection for crop improvement: current progress and future prospects[J]. Molecular Genetics and Genomics, 2023, 298: 813-821. DOI:10.1007/s00438-023-02026-0.
[5] VAN EIJNATTEN A L, STERKEN M G, KAMMENGA J E, et al. The effect of developmental variation on expression QTLs in a multi parental Caenorhabditis elegans population[J]. G3: Genes|Genomes|Genetics, 2024, 14(2): jkad273. DOI:10.1093/g3journal/jkad273.
[6] JANSEN R C, NAP J P.Genetical genomics: the added value from segregation[J]. Trends in Genetics, 2001, 17(7): 388-391. DOI:10.1016/S0168-9525(01)02310-1.
[7] ZHANG L, LU D, GE X, et al.Insight into growth and wood properties based on QTL and eQTL mapping in Populus deltoides ‘Danhong’ × Populus simonii ‘Tongliao1’[J]. Industrial Crops & Products, 2023, 199: 116731. DOI:10.1016/j.indcrop.2023.116731.
[8] LANGFELDER P, HORVATH S.WGCNA: an R package for weighted correlation network analysis[J]. BMC Bioinformatics, 2008, 9: 559. DOI:10.1186/1471-2105-9-559.
[9] LIANG J, WU Z, ZHANG X, et al.Study on the interactions of cyclins with CDKs involved in auxin signal during leaf development by WGCNA in Populus alba[J]. International Journal of Molecular Sciences, 2023, 24(17): 13445. DOI:10.3390/ijms241713445.
[10] WANG R, XUE Y, FAN J, et al.A systems genetics approach reveals PbrNSC as a regulator of lignin and cellulose biosynthesis in stone cells of pear fruit[J]. Genome Biology, 2021, 22(1): 313. DOI:10.1186/s13059-021-02531-8.
[11] PENG L, LI Y, TIAN W, et al. Combined genome-wide association studies and expression quantitative trait locus analysis uncovers a genetic regulatory network of floral organ number in a tree peony (Paeonia suffruticosa Andrews) breeding population[J]. Horticulture Research, 2023, 10(7): uhad110. DOI:10.1093/hr/uhad110.
[12] 周志春. 中国木荷[M]. 北京: 科学出版社, 2021: 3-5.
ZHOU Z C.Schima superba in China[M]. Beijing: Science Press, 2021: 3-5.
[13] 王云鹏, 张蕊, 周志春, 等. 木荷优树自由授粉家系早期生长性状遗传变异动态规律[J]. 林业科学, 2020, 56(9): 77-86. DOI:10.11707/j.1001-7488.20200909.
WANG Y P, ZHANG R, ZHOU Z C, et al.Dynamic patterns of genetic variation in early growth traits of the open-pollinated families of Schima superba plus trees[J]. Scientia Silvae Sinicae, 2020, 56(9): 77-86. DOI:10.11707/j.1001-7488.20200909.
[14] 欧阳天林, 朱柯帆, 邱建勋, 等. 木荷种子园自由授粉家系生长遗传变异及初选[J]. 中南林业科技大学学报, 2022, 42(9): 17-23. DOI:10.14067/j.cnki.1673-923X.2022.09.003.
OUYANG T L, ZHU K F, QIU J X, et al.Genetic variation and selection of the free-pollinated families in Schima superba seed orchard[J]. Journal of Central South University of Forestry & Technology, 2022, 42(9): 17-23. DOI:10.14067/j.cnki.1673-923X.2022.09.003.
[15] BOLGER A M, LOHSE M, USADEL B.Trimmomatic: a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014, 30(15): 2114-2120. DOI:10.1093/bioinformatics/btu170.
[16] DOBIN A, DAVIS C A, SCHLESINGER F, et al.STAR: ultrafast universal RNA-seq aligner[J]. Bioinformatics, 2013, 29(1): 15-21. DOI:10.1093/bioinformatics/bts635.
[17] LIAO Y, SMYTH G K, SHI W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features[J]. Bioinformatics, 2014, 30(7): 923-930. DOI:10.1093/bioinformatics/btt656.
[18] LI H, DURBIN R.Fast and accurate short read alignment with Burrows-Wheeler transform[J]. Bioinformatics, 2009, 25(14): 1754-1760. DOI:10.1093/bioinformatics/btp324.
[19] LI H, HANDSAKER B, WYSOKER A, et al.The Sequence Alignment/Map format and SAMtools[J]. Bioinformatics, 2009, 25(16): 2078-2079. DOI:10.1093/bioinformatics/btp352.
[20] STEGLE O, PARTS L, PIIPARI M, et al.Using probabilistic estimation of expression residuals (PEER) to obtain increased power and interpretability of gene expression analyses[J]. Nature Protocols, 2012, 7: 500-507. DOI:10.1038/nprot.2011.457.
[21] SHABALIN A A.Matrix eQTL: ultra fast eQTL analysis via large matrix operations[J]. Bioinformatics, 2012, 28(10): 1353-1358. DOI:10.1093/bioinformatics/bts163.
[22] CHEN L, LIU L, YANG G, et al.Expression quantitative trait locus of wood formation-related genes in Salix suchowensis[J]. International Journal of Molecular Sciences, 2024, 25: 247. DOI:10.3390/ijms25010247.
[23] SZKLARCZYK D, KIRSCH R, KOUTROULI M, et al.The STRING database in 2023: protein-protein association networks and functional enrichment analyses for any sequenced genome of interest[J]. Nucleic Acids Research, 2023, 51(D1): D638-D646. DOI:10.1093/nar/gkac1000.
[24] 陆艳, 王旭军, 粟俊榕, 等. 杉木无性系生长和干形性状的遗传变异及多性状指数选择[J]. 湖南林业科技, 2024, 51(4): 19-26. DOI:10.3969/j.issn.1003-5710.2024.04.003.
LU Y, WANG X J, SU J R, et al.Genetic variation and multi-trait index selection of growth and stem form traits in Chinese fir clones[J]. Hunan Forestry Science & Technology, 2024, 51(4): 19-26. DOI:10.3969/j.issn.1003-5710.2024.04.003.
[25] 李昌荣, 陈健波, 郭东强, 等. 锯材大花序桉生长和材性的综合指数选择[J]. 南京林业大学学报(自然科学版), 2019, 43(1): 1-8. DOI:10.3969/j.issn.1000-2006.201805018.
LI C R, CHEN J B, GUO D Q, et al.Comprehensive index selection on superior growth and wood properties of Eucalyptus cloeziana for saw timber[J]. Journal of Nanjing Forestry University (Natural Sciences Edition), 2019, 43(1): 1-8. DOI:10.3969/j.issn.1000-2006.201805018.
[26] WANG X, CHEN Q, WU Y, et al.Genome-wide analysis of transcriptional variability in a large maize-teosinte population[J]. Molecular Plant, 2018, 11(3): 443-459. DOI:10.1016/j.molp.2017.12.011.
[27] KLIEBENSTEIN D.Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs[J]. Annual Review of Plant Biology, 2009, 60: 93-114. DOI:10.1146/annurev.arplant.043008.092114.
[28] LIU S, LI C, WANG H, et al.Mapping regulatory variants controlling gene expression in drought response and tolerance in maize[J]. Genome Biology, 2020, 21(1): 163. DOI:10.1186/s13059-020-02069-1.
[29] NIEUWLAND J, SCOFIELD S, MURRAY J A.Control of division and differentiation of plant stem cells and their derivatives[J]. Seminars in Cell & Developmental Biology, 2009, 20(9): 1134-1142. DOI:10.1016/j.semcdb.2009.09.011.
[30] ZHENG T, DAI L, LI S, et al.Populus D-type cyclin gene PsnCYCD1;1 accelerates cell division and participates in secondary growth of vascular bundles[J]. Journal of Experimental Botany, 2023, 74(14): 4077-4092. DOI:10.1093/jxb/erad140.
[31] DUBOS C, STRACKE R, GROTEWOLD E, et al.MYB transcription factors in Arabidopsis[J]. Trends in Plant Science, 2010, 15(10): 573-581. DOI:10.1016/j.tplants.2010.06.005.
[32] FENG G, BURLEIGH J G, BRAUN E L, et al.Evolution of the 3R-MYB gene family in plants[J]. Genome Biology and Evolution, 2017, 9(4): 1013-1029. DOI:10.1093/gbe/evx056.
[33] ITO M, ARAKI S, MATSUNAGA S, et al.G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors[J]. The Plant Cell, 2001, 13(8): 1891-1905. DOI:10.1105/TPC.010102.
[34] HAGA N, KATO K, MURASE M, et al.R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana[J]. Development, 2007, 134(6): 1101-1110. DOI:10.1242/dev.02801.
[35] HAGA N, KOBAYASHI K, SUZUKI T, et al.Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/M-specific genes in Arabidopsis[J]. Plant Physiology, 2011, 157(2): 706-717. DOI:10.1104/pp.111.180836.
[36] 张薇, 赵礼轲, 张丙林, 等. 植物特异性HD-Zip转录因子在生长发育与逆境响应中的功能研究进展[J]. 生命科学, 2025, 37(6): 625-634. DOI:10.13376/j.cbls/2025062.
ZHANG W, ZHAO L K, ZHANG B L, et al.Research advances in the roles of plant-specific HD-Zip transcription factors in growth, development, and stress response[J]. Chinese Bulletin of Life Sciences, 2025, 37(6): 625-634. DOI:10.13376/j.cbls/2025062.
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