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Acta Agron Sin ›› 2016, Vol. 42 ›› Issue (09): 1319-1331.doi: 10.3724/SP.J.1006.2016.01319


Transcriptome Analysis of Stem Morphogenesis Under Shade Stress in Soybean

REN Meng-Lu1,LIU Wei-Guo1,*,LIU Ting1,DU Yong-Li1,DENG Yu-Chuan1,ZOU Jun-Lin2,YUAN Jin3,YANG Wen-Yu1,*   

  1. 1 Institute of Ecological Agriculture, Sichuan Agricultural University / Key Laboratory of Crop Ecophysiology and Farming System in Southwest China, Ministry of Agriculture, Chengdu 611130, China; 2 Bureau of Rural Economic Development, Pengzhou 611930, China; 3 The Seed Management Station, Chengdu 610041, China
  • Received:2016-01-11 Revised:2016-03-14 Online:2016-09-12 Published:2016-03-28
  • Contact: 刘卫国, E-mail: lwgsy@126.com, Tel: 028-86290960; 杨文钰, E-mail: mssiyangwy@sicau.edu.cn, Tel: 0835-2882004 E-mail:1461755144@qq.com
  • Supported by:

    This study was supported by Sichuan Crop Breeding Key Project.


Maize-soybean relay-cropping system is a key technology in agriculture, studying the molecular mechanisms for shade stress responses of soybean grown in the intercropping system will be useful for soybean improvement by genetic manipulation. An experiment was conducted using two different shade susceptive soybean (Glycine max L.) varieties Nandou 12 and Nan032-4 to investigate the transcriptome changes in response to shade stress by RNA-seq technology. The results indicated that 287 differentially expressed genes in Nandou12 and 110 the genes in Nan032-4 were significantly affected by shade, and the expression of the genes was mainly up-regulated. Gene ontology analyses showed that differentially expressed genes were enriched in secondary cell wall biogenesis, polysaccharides synthesis, calmodulin binding, hydrolase activity and so on. In the shade treatment, differentially expressed genes responded to lignin and auxin biosynthetic processes were up-regulated in Nandou 12; and genes responded to jasmonic acid and ethylene biosynthetic processes were up-regulated, but genes responded to gibberellin metabolic process were down-regulated in Nan 032-4. However, Nandou 12 had more differentially expressed genes than Nan 032-4. The accumulateion of polysaccharides in cell wall and acceleration of secondary cell wall formation hindered the radial growth of stem making stem thinner, meanwhile the increase of hydrolysis enzyme activity accelerated the relaxation of cells, making stem longer. Nandou12 and Nan032-4 also had their particular genes to response shade, but Nandou 12 had more cell wall polysaccharides, lignin content and auxin content to increase the intensity of stem keeping a certain morphological advantage, resulting in higher lodging resistance under the shade, that is a stronger adaptability to shade.

Key words: Soybean, Replay strip intercropping, Shade stress, Stem, Transcriptome

[1]  杨文钰, 雍太文, 任万军, 樊高琼, 牟锦毅, 卢学兰. 发展套作大豆, 振兴大豆产业. 大豆科学, 2008, 27(1): 1–7
Yang W Y, Yong T W, Ren W J, Fan G Q, Mu J Y, Lu X L. Develop relay–planting soybean, revitalize soybean industry. Soybean Sci, 2008, 27(1): 1–7 (in Chinese with English abstract)
[2]  刘广才. 不同间套作系统种间营养竞争的差异性及其机理研究.甘肃农业大学, 甘肃兰州, 2005
Liu G C. Difference and its mechanism of interspecific nutrition competition in different intercropping systems, PhD Dissertation of Gansu Agricultural University, Lanzhou, China, 2005 (in Chinese with English abstract)
[3]  Kayhan F, Pierre D, Donald S. Soybean canopy development as affected by population density and intercropping with corn, Fractal analysis in comparison with other quantitative approaches. Crop Sci, 1999, 39: 1784–1791
[4]  Liu W G, Zou J L, Zhang J, Yang F, Wan Y, Yang W Y. Evaluation of soybean (Glycine max) stem vining in maize–soybean relay strip intercropping system. Plant Prod Sci, 2015, 18: 69–75
[5]  吴雨珊, 龚万灼, 廖敦平, 武晓玲, 杨峰, 刘卫国, 雍太文, 杨文钰. 带状套作荫蔽及复光对不同大豆品种(系)生长及产量的影响. 作物学报, 2015, 41: 1740–1747
Wu Y S, Gong W Z, Liao D P, Wu X L, Yang F, Liu W G, Yong T W, Yang W Y. Effects of shade and light recovery on soybean cultivars (lines) and its relationship with yield in relay strip intercropping system. Acta Agron Sin, 2015, 41: 1740–1747 (in Chinese with English abstract)
[6]  刘卫国, 蒋涛, 佘跃辉, 杨峰, 杨文钰. 大豆苗期茎秆对阴蔽胁迫响应的生理机制初探. 中国油料作物学报, 2011, 33(2): 141–146
Liu W G, Jiang T, She Y H, Yang F, Yang W Y. Preliminary study on physiological response mechanism of soybean (Glycine max) stem to shade stress at seedling stag. Chin J Oil Crop Sci, 2011, 33(2): 141–146 (in Chinese with English abstract)
[7]  王一, 杨文钰, 张霞, 雍太文, 刘卫国, 苏本营. 不同生育时期遮阴对大豆形态性状和产量的影响. 作物学报, 2013, 39: 1871–1879
Wang Y, Yang W Y, Zhang X, Yong T W, Liu W G, Su B Y. Effects of shading at different growth stages on different traits and yield of soybean. Acta Agron Sin, 2013, 39: 1871–1879 (in Chinese with English abstract)
[8]  Wang J, Zhu J, Lin Q Q, Li X J, Teng N J, Li Z S, Li B, Zhang A, Lin J X. Effects of stem structure and cell wall components on bending strength in wheat. Chin Sci Bull, 2006, 51: 815–823
[9]  勾玲, 赵明, 黄建军, 张宾, 李涛, 孙锐. 玉米茎秆弯曲性能与抗倒能力的研究. 作物学报, 2008, 34: 653−661
Gou L, Zhao M, Huang J J, Zhang B, Li T, Sun R. Bending Mechanical Properties of Stalk and Lodging-Resistance of Maize (Zea mays L.). Acta Agron Sin, 2008, 34: 653−661 (in Chinese with English abstract)
[10] Dhugga K S. Plant golgi cell wall synthesis: From genes to enzyme activities. Proc Natl Acad Sci USA, 2005, 102: 1815–1816
[11] 王庭杰, 张亮, 韩琼, 郑凤霞, 王天琪, 冯娜娜, 王太霞. 玉米茎秆细胞壁和组织构建对抗压强度的影响. 植物科学学报, 2015, 33: 109–115
Wang T J, Zhang L, Han Q, Zheng F X, Wang T Q, Feng N N, Wang T X. Effects of stalk cell wall and tissue on the compressive strength of maize. Plant Sci J, 2015, 33: 109–115 (in Chinese with English abstract)
[12] 陈年来, 胡敏, 乔昌萍, 乃小英, 王锐. BTH、SA和SiO2处理对甜瓜幼苗白粉病抗性及叶片HRGP和木质素含量的影响. 中国农业科学, 2010, 43: 535–541
Chen N L, Hu M, Qiao C P, Nai X Y, Wang R. Effects of BTH, SA, and SiO2 treatment on disease resistance and leaf HRGP and lignin contents of melon seedlings. Sci Agric Sin, 2010, 43: 535–541 (in Chinese with English abstract)
[13] 邹俊林, 刘卫国, 袁晋, 蒋涛, 叶素琴, 邓榆川, 杨晨雨, 罗玲, 杨文钰. 套作大豆苗期茎秆木质素合成与抗倒性的关系. 作物学报, 2015, 41: 1098–1104
Zou J L, Liu W G, Yun J, Jiang T, Ye S Q, Deng Y C, Yang C Y, Luo L, Yang W Y. Relationship between lignin synthesis and lodging resistance at seedlings stage in soybean intercropping system. Acta Agron Sin, 2015, 41: 1098–1104 (in Chinese with English abstract)
[14] 齐秀东, 魏建梅, 高海生, 贾艳茹, 张海娥. 梨果实发育软化与果胶多糖降解特性的关系. 中国农业科学, 2015, 48: 3027–3037
Qi X D, Wei J M, Gao H S, Jia Y R, Zhang H E. Pectin polysaccharide degradation in relation to the texture softening in pear fruit. Sci Agric Sin, 2015, 48: 3027–3037 (in Chinese with English abstract)
[15] Vicky S T, Van S, Dmitry S, Jean-pierre V, Kris V. Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot, 2007, 100: 1467–1473
[16] 罗玲, 于晓波, 万燕, 蒋涛, 杜俊波, 邹俊林, 杨文钰, 刘卫国. 套作大豆苗期倒伏与茎秆内源赤霉素代谢的关系. 中国农业科学, 2015, 48: 2528–2537
Luo L, Yu X B, Wan Y, Jiang T, Du J B, Zou J L, Yang W Y, Liu W G. The relationship between lodging and stem endogenous gibberellins metabolism pathway of relay intercropping soybean at seedling stage. Sci Agric Sin, 2015, 48: 2528–2537 (in Chinese with English abstract)
[17] Kurepin L V, Walton L J, Reid D. Interaction of red to far red light ratio and ethylene in regulating stem elongation of Helianthus annuus. Plant Growth Regul, 2007, 51(1): 53–61
[18] 宫长荣, 李艳梅, 杨立均. 水分胁迫下离体烟叶中脂氧合酶活性、水杨酸与茉莉酸积累的关系. 中国农业科学, 2003, 36: 269–272
Gong C R, Li Y M, Yang L J. Relationship between LOX activity and SA and JA accumulations in tobacco leave under water stress. Sci Agric Sin, 2003, 36: 269–272 (in Chinese with English abstract)
[19] Liu H, Ou-yang B, Zhang J H, Wang T T, Li H X, Zhang Y Y, Yu C Y, Ye Z H. Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PloS One, 2012, 7(11): e50785
[20] Fullwood M J, Wei C L, Liu E T, Ruan Y. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res, 2009, 19: 521–532
[21] Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shino-zaki K. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Plant Biol, 2006, 17: 113–122
[22] Valliyodan B, Nguyen H T. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol, 2006, 9: 189–195
[23] Colebatch G S, Kloska B, Trevaskis B. Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol. Plant Microbe Interact, 2002, 15: 411–420
[24] Severin A J, Woody J L, Bolon Y T. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol, 2010, 10: 160–165
[25] Keurentjes J J, Fu J. Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci. Proc Natl Acad Sci USA, 2007, 104: 1708–1713
[26] Liu W G, Jiang T, Zhou X R, Yang W Y. Characteristics of expansins in soybean (Glycine max) internodes and responses to shade stress. Asian J Crop Sci, 2011, 3: 26–34
[27] 李长宁, 谢金兰, 王维赞, 李毅杰, 梁强, 董文斌, 刘晓燕, 杨丽涛, 李杨瑞. 水分胁迫下甘蔗差异表达基因筛选及激素相关基因分析. 作物学报, 2015, 41: 1127–1135
Li C N, Xie J L, Wang W Z, Li Y J, Liang Q, Dong W B, Liu X Y, Li Y R. Screening of differentially expressed genes and analysis of plant hormones related genes under water stress in sugarcane. Acta Agron Sin, 2015, 41: 1127–1135 (in Chinese with English abstract)
[28] Shinozaki K, Yamaguchi-Shinozaki K. Gene expression and signal transduction in water-stress response. Plant Physiol, 1997, 115: 327–334
[29] Yang F, Huang S, Gao R C, Liu W G, Yong T W, Wang X C, Wu X L, Yang W Y. Growth of soybean seedlings in relay strip intercropping systems in relation to light quantity and red: far-red ratio. Field Crops Res, 2014, 155: 245–253
[30] 丁宝莲, 谈宏鹤, 朱素琴. 胁迫与植物细胞壁关系研究进展. 广西科学院学报, 2001, 17(2): 87–90
Ding B L, Tan H H, Zhu S Q. Advances on research of the relationship between stresses and plant cell wall. J Guangxi Acad Sci, 2001, 17(2): 87–90 (in Chinese with English abstract)
[31] 李家宝. 棉花类成束蛋白阿拉伯半乳聚糖蛋白基因(GhFLA)的克隆与功能分析. 西南大学博士学位论文, 重庆, 2007
Li J B. Cloning and Function Analysis of Fasciclin-like Arabinogalactanprotein Gene (GhFLA) from Cotton. PhD Dissertation of Southwest University, Chongqing, China, 2007 (in Chinese with English abstract)
[32] Andeme-Onzighi C, Sivaguru M, Judy-March J, Baskin T I, Driouich A. The reb1-1 mutation of Aribdopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubles. Planta, 2002, 215: 949–958
[33] Park M H, Suzuky Y, Chono M, Knox J P, Yamaguchi I. CsAGP1, a gibberellin-response gene from cucumber hypocotyls, encodes a classical arabinogalactan protein and is involved in stem elongation. Plant Physiol, 2003, 135: 1450–1459
[34] Shi H, Kim Y, Guo Y, Stevenson B, Zhu J K. The Aribidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell, 2003, 15: 19–23
[35] Itom S, Suzhuky Y, Miyamoto K, Ueda J, Yamaguchi I. At-FLA11, a fasciclin-like arabinogalactan-protein, specifically localized in sclerenchyma cells. Biosci Biotechnol Biochem, 2005, 69: 1963–1969
[36] Fry S C, Smith R C, Renwick K F, Martin D J, Hodge S K, Matthews K J. Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J, 1992, 282(3): 821–828
[37] Nishitani K, Tominaga R. Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem, 1992, 267: 21058–21064
[38] Hyodo H, Yamakawa S, Takeda Y, Tsuduki M, Yokota A, Nishitani K, Kohchi T. Active gene expression of a xyloglucan endo-transglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol Biol, 2003, 52: 473–482
[39] Jan A, Yang G, Nakamura H, Ichikawa H, Kitano H, Matsuoka M, Matsumoto H, Komatsu S. Characterization of a xyloglucan endotransglucosylase gene that is up-regulated by gibberellin in rice. Plant Physiol, 2004, 136: 3670–3681
[40] 李健. 转脂质转运蛋白基因山新杨抗逆性分析. 东北林业大学博士学位论文, 黑龙江哈尔滨, 2010
Li J. The Analysis of Abiotic Stress Resistence of Tansgenic Populus davidiana Dode P. Bollena Lauche Overexpressing ThLTP Gene. PhD Dissertation of Northeast Agricultural University, Heilongjiang, China, 2010 (in Chinese with English abstract)

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