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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (3): 385-394.doi: 10.3724/SP.J.1006.2020.93021

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS • Previous Articles     Next Articles

Identification of gene co-expression modules of maize plant height and ear height by WGCNA

Juan MA,Yan-Yong CAO,Li-Feng WANG,Jing-Jing LI,Hao WANG,Yan-Ping FAN,Hui-Yong LI()   

  1. Institute of Cereal Crops, Henan Academy of Agricultural Sciences, Zhengzhou 450002, Henan, China
  • Received:2019-04-02 Accepted:2019-09-26 Online:2020-03-12 Published:2020-03-01
  • Contact: Hui-Yong LI E-mail:lihuiyong1977@126.com
  • Supported by:
    This study was supported by the National Key Research and Development Program of China(2016YFD100103);the Science and Technology Project of Henan province(192102110008)

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Abstract:

Plant height (PH) and ear height (EH) are important factors for maize plant type and grain yield. Weighted gene co-expression network analysis (WGCNA) is an important method to explain the relationships between gene network and complicated traits and identify the PH and EH associated genes. In this study, we used Zheng 58, Ye 478, Chang 7-2, Huangzaosi and its combinations Zhengdan 958, Anyu 5, Zheng 58/Huangzaosi, and Ye 478/Huangzaosi as materials and utilized transcriptome data under the planting densities of 45,000 plants hm -2and 67,500 plants hm -2 to construct a co-expression network by WGCNA, getting 24 and 21 co-expression modules, respectively. Among them, a total of 15 co-expression modules were significantly correlated with PH and EH, with the absolute correlation coefficients higher than 0.50. Six modules were overlapped between PH and EH. By gene function analysis, these overlapped modules were significantly enriched in development, photosynthesis, response to light stimulus, plant hormone, and carbohydrate biosynthesis/metabolism related activities. According to connectivity of genes in modules, AP2-EREBP transcription factor EREB14, thiaminase TENA2, phosphoglyceric kinase PGK, glutathione transferase GST2, and succinate dehydrogenase SUDH7 were considered as hub genes. From gene networks, EREB14 was connected with three known PH genes D8, DWF1, ZmGRF10, and C3H35 (C3H transcription factor), GATA4 (C2C2-GATA transcription factor), and ethylene homology ETR40. Reported PH genes An1 and GA20ox3 were also found in our co-expression modules. From the networks of the five known PH genes, ARF-transcription factor 7 (ARFTF7), ARFTF26, GST39, photosystem II oxygen evolving polypeptide PspB2, and photosystem I N subunit PasN1 had connections with these known PH genes. The identification of 15 co-expression modules and their hub genes, and analysis of their gene function and gene networks of key genes will be helpful for revealing the genetic basis of PH and EH.

Key words: maize, weighted gene co-expression network, transcriptome, plant height, ear height

Fig. 1

Determination of soft threshold β at 45,000 plants hm-2 (A) and 67,500 plants hm-2 (B) A and B: The ordinate represents the index of scale free network model in left figure. The ordinate represents the average link degree of each soft threshold in right figure. The abscissa represents the soft threshold β."

Fig. 2

Plant height and ear height of eight materials at 45,000 plants hm-2 and 67,500 plants hm-2 Number represents mean±SE. Bars with different letters are significantly different at P < 0.05 as determined by Duncan’s multiple comparison. * denotes significant at the 0.05 probability level."

Fig. 3

Gene cluster dendrograms and modules construction at 45,000 plants hm-2(A) and 67,500 plants hm-2 (B)"

Fig. 4

Co-expression modules, gene number, and correlation coefficient for plant height (PH) and ear height (EH) at 45,000 plants hm-2"

Fig. 5

Co-expression modules, gene number, and correlation coefficient for plant height (EH) and ear height (EH) at 67,500 plants hm-2"

Fig. 6

Gene networks of hub genes for significant co-expression modules Colors in figure represent Turquoise, Lightgreen, and Pink modules."

Fig. 7

Gene networks of known plant height genes D8, DWF1, ZmGRF10, An1, and GA20ox3 Colors in figure represent Turquoise, Brown, and Pink modules."

[1] 李清超, 李永祥, 杨钊钊, 刘成, 刘志斋, 李春辉, 彭勃, 张岩, 王迪, 谭巍巍, 孙宝成, 石云素, 宋燕春, 张志明, 潘光堂, 黎裕, 王天宇 . 基于多重相关RIL群体的玉米株高和穗位高QTL定位. 作物学报, 2013,39:1521-1529.
Li Q C, Li Y X, Yang Z Z, Liu C, Liu Z Z, Li C H, Peng B, Zhang Y, Wang D, Tan W W, Sun B C, Shi S Y, Song C Y, Zhang Z M, Pan G T, Li Y, Wang T Y . QTL mapping for plant height and ear height by using multiple related RIL populations in maize. Acta Agron Sin, 2013,39:1521-1529 (in Chinese with English abstract).
[2] 何坤辉, 常立国, 崔婷婷, 渠建洲, 郭东伟, 徐淑兔, 张兴华, 张仁和, 薛吉全, 刘建超 . 多环境下玉米株高和穗位高的QTL定位. 中国农业科学, 2016,49:1443-1452.
He K H, Chang L G, Cui T T, Qu J Z, Guo D W, Xu S T, Zhang X H, Zhang R H, Xue J Q, Liu J C . Mapping QTL for plant height and ear height in maize under multi-environments. Sci Agric Sin, 2016,49:1443-1452 (in Chinese with English abstract).
[3] 刘坤, 张雪海, 孙高阳, 闫鹏帅, 郭海平, 陈思远, 薛亚东, 郭战勇, 谢惠玲, 汤继华, 李卫华 . 玉米株型相关性状的全基因组关联分析. 中国农业科学, 2018,51:821-834.
Liu K, Zhang X H, Sun G Y, Yan P S, Guo H P, Chen S Y, Xue Y D, Guo Z Y, Xie H L, Tang J H, Li W H . Genome-wide association studies of plant type traits in maize. Sci Agric Sin, 2018,51:821-834 (in Chinese with English abstract).
[4] 李凯, 张晓祥, 管中荣, 沈亚欧, 潘光堂 . 玉米株高和穗位高的全基因组关联分析. 玉米科学, 2017,25(6):1-7.
Li K, Zhang X X, Guan Z R, Shen Y O, Pan G T . Genome-wide association analysis of plant height and ear height in maize. J Maize Sci, 2017,25(6):1-7 (in Chinese with English abstract).
[5] Li X, Zhou Z, Ding J, Wu Y, Zhou B, Wang R, Ma J, Wang S, Zhang X, Xia Z, Chen J, Wu J . Combined linkage and association mapping reveals QTL and candidate genes for plant and ear height in maize. Front Plant Sci, 2016,7:833.
[6] Weng J, Xie C, Hao Z, Wang J, Liu C, Li M, Zhang D, Bai L, Zhang S, Li X . Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS One, 2011,6:e29229.
[7] Fujioka S, Yamane H, Spray C R, Gaskin P, Macmillan J, Phinney B O, Takahashi N . Qualitative and quantitative analyses of gibberellins in vegetative shoots of normal, dwarf-1, dwarf-2, dwarf-3, and dwarf-5 seedlings of Zea mays L. Plant Physiol, 1988,88:1367-1372.
[8] Winkler R G, Helentjaris T . The maize Dwarf3 gene encodes acytochrome P450-mediated early step in gibberellin biosynthesis. Plant Cell, 1995,7:1307-1317.
[9] Thornsberry J M, Goodman M M, Doebley J, Kresovich S, Nielsen D, Buckler E S . Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet, 2001,28:286-289.
[10] Lawit S J, Wych H M, Xu D, Kundu S, Tomes D T . Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol, 2010,51:1854-1868.
[11] Multani D S, Briggs S P, Chamberlin M A, Blakeslee J J, Murphy A S, Johal G S . Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science, 2003,302:81-84.
[12] Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol, 2005, 4: Article 17.
[13] Zhang X, Hirsch C N, Sekhon R S, De Leon N, Kaeppler S M . Evidence for maternal control of seed size in maize from phenotypic and transcriptional analysis. J Exp Bot, 2016,67:1907-1917.
[14] Ma J, Zhang D, Cao Y, Wang L, Li J, Lübberstedt T, Wang T, Li Y, Li H . Heterosis-related genes under different planting densities in maize (Zea mays L.). J Exp Bot, 2018,69:5077-5087.
[15] Zhan J, Thakare D, Ma C, Lloyd A, Nixon N M, Arakaki A M, Burnett W J, Logan K O, Wang D, Wang X, Drews G N, Yadegari R . RNA sequencing of laser-capture microdissected compartments of the maize kernel identifies regulatory modules associated with endosperm cell differentiation. Plant Cell, 2015,27:513-531.
[16] 杨宇昕, 桑志勤, 许诚, 代文双, 邹枨 . 利用WGCNA进行玉米花期基因共表达模块鉴定. 作物学报, 2019,45:161-174.
Yang Y X, Sang Z Q, Xu C, Dai W S, Zou C . Identification of maize flowering gene co-expression modules by WGCNA. Acta Agron Sin, 2019,45:161-174 (in Chinese with English abstract).
[17] Peng H, He X, Gao J, Ma H, Zhang Z, Shen Y, Pan G, Lin H . Transcriptomic changes during maize roots development responsive to Cadmium (Cd) pollution using comparative RNA seq- based approach. Biochem Biophys Res Commun, 2015,464:1040-1047.
[18] Thirunavukkarasu N, Hossain F, Mohan S, Shiriga K, Mittal S, Sharma R, Singh R K, Gupta H S . Genome-wide expression of transcriptomes and their co-expression pattern in subtropical maize (Zea mays L.) under waterlogging stress. PLoS One, 2013,8:e70433.
[19] Lyu Y, Liang Z, Ge M, Qi W, Zhang T, Lin F, Peng Z, Zhao H . Genome-wide identification and functional prediction of nitrogen-responsive intergenic and intronic long non-coding RNAs in maize ( Zea mays L.). BMC Genomics, 2016,17:350.
[20] Zhang S, Yang W, Zhao Q, Zhou X, Jiang L, Ma S, Liu X, Li Ye, Zhang C, Fan Y, Chen R . Analysis of weighted co-regulatory networks in maize provides insights into new genes and regulatory mechanisms related to inositol phosphate metabolism. BMC Genomics, 2016,17:129-146.
[21] Tao Y, Zheng J, Xu Z, Zhang X, Zhang K, Wang G . Functional analysis of ZmDWF1, a maize homolog of the Arabidopsis brassinosteroids biosynthetic DWF1/DIM gene. Plant Sci, 2004,167:741-751.
[22] Wu L, Zhang D, Xue M, Qian J, He Y, Wang S . Overexpression of the maize GRF10, an endogenous truncated growth regulating factor protein, leads to reduction in leaf size and plant height. J Integr Plant Biol, 2014,56:1053-1063.
[23] Hartwig T, Chuck G S, Fujioka S, Klempien A, Weizbauer R, Potluri D P, Choe S, Johal G S, Schulz B . Brassinosteroid control of sex determination in maize. Proc Natl Acad Sci USA, 2011,108:19814-19819.
[24] Tamotsu H, Rod W K, Chris A H, Masaji K . The involvement of gibberellin 20-oxidase genes in phytochrome-regulated petiole elongation of Arabidopsis. Plant Physiol, 2005,138:1106-1116.
[25] Zhao W, Langfelder P, Fuller T, Dong J, Li A, Hovarth S . Weighted gene coexpression network analysis: state of the art. J Biopharm Stat, 2010,20:281-300.
[26] Wang H, Gu L, Zhang X, Liu M, Jiang H, Cai R, Zhao Y, Cheng B . Global transcriptome and weighted gene co-expression network analyses reveal hybrid-specific modules and candidate genes related to plant height development in maize. Plant Mol Biol, 2018,98:187-203.
[27] Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K . AP2/ERF family transcription factors in plant abiotic stress responses. BBA-Gene Regul Mech, 2012,1819:86-96.
[28] Hinz M, Wilson I W, Yang J, Buerstenbinder K, Llewellyn D, Dennis E S, Sauter M, Dolferus R . Arabidopsis RAP2: 2. An ethylene response transcription factor that is important for hypoxia survival. Plant Physiol, 2010,153:757-772.
[29] Licausi F, Ohme Takagi M, Perata P . APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol, 2013,199:639-649.
[30] Cassani E, Bertolini E, Cerino B F, Landoni M, Gavina D, Sirizzotti A, Pilu R . Characterization of the first dominant dwarf maize mutant carrying a single amino acid insertion in the VHYNP domain of the dwarf8 gene. Mol Breed, 2009,24:375-385.
[31] Teng F, Zhai L, Liu R, Bai W, Wang L, Huo D, Tao Y, Zheng Y, Zhang Z . ZmGA3ox2, a candidate gene for a major QTL, qPH3.1, for plant height in maize. Plant J, 2013,73:405-416.
[32] 郑雷, 周羽, 曾兴, 邸宏, 翁建峰, 李新海, 王振华 . 玉米株高QTL定位研究进展. 作物杂志, 2016, ( 2):8-13.
Zheng L, Zhou Y, Zeng X, Di H, Weng J F, Li X H, Wang Z H . QTL Mapping of plant height in maize. Crops, 2016, ( 2):8-13 (in Chinese with English abstract).
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