Please wait a minute...
Journal of Integrative Agriculture  2019, Vol. 18 Issue (9): 2029-2040    DOI: 10.1016/S2095-3119(18)62123-9
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
iTRAQ protein profile analysis of soybean stems reveals new aspects critical for lodging in intercropping systems
LIU Wei-guo*, WEN Bing-xiao*, ZHOU Tao, WANG Li, GAO Yang, LI Shu-xian, QIN Si-si, LIU Jiang, YANG Wen-yu
Institute of Ecological Agriculture, Sichuan Agricultural University/Sichuan Engineering Research Center for Crop Strip Intercropping System, Chengdu 611930, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Soybean is often intercropped with maize, sugarcane, and sorghum.  Because of the shade coming from the latter, the soybean stem lodging is often a very serious problem in intercropping systems.  The aim of this study is to characterize the possible mechanisms in the stem of shade-induced promotion of seedling soybean lodging in intercropping systems at the proteome level.  We found that the soybean stem became slender and prone to lodging when it was planted with maize in an intercropping system.  The inhibition of lignin biosynthesis and lack of photosynthate (soluble sugar) for the biosynthesis of the cell wall led to the lower internode breaking strength.  A total of 317 proteins were found to be affected in the soybean stem in response to shade.  Under the shade stress, the down-expression of key enzymes involving the phenylpropanoid metabolic pathway inhibited lignin biosynthesis.  The up-regulation of expansin and XTHs protein expression relaxed the cell wall and promoted the elongation of internodes.  Although the expression of the enzymes involving sucrose synthesis increased in the soybean stem, the lack of a carbon source prevented rapid stem growth.  This metabolic deficit is the principal cause of the lower cellulose content in the stem of intercropped soybean, which leads to weakened stems and a propensity for lodging.
Keywords:  soybean        lodging        intercropping        shade stress        lignin  
Received: 20 May 2018   Accepted:
Fund: This research was supported by the National Natural Science Foundation of China (31671626 and 31201170).
Corresponding Authors:  Correspondence YANG Wen-yu, E-mail:   
About author:  * These authors contributed equally to this study.

Cite this article: 

LIU Wei-guo, WEN Bing-xiao, ZHOU Tao, WANG Li, GAO Yang, LI Shu-xian, QIN Si-si, LIU Jiang, YANG Wen-yu. 2019. iTRAQ protein profile analysis of soybean stems reveals new aspects critical for lodging in intercropping systems. Journal of Integrative Agriculture, 18(9): 2029-2040.

Awal M A, Koshi H, Ikeda T. 2006. Radiation interception and use by maize/peanut intercrop canopy. Agricultural and Forest Meteorology, 139, 74–83.
Bhaskara Reddy M V, Arul J, Angers P, Couture L. 1999. Chitosan treatment of wheat seeds induces resistance to Fusarium graminearum and improves seed quality. Journal of Agricultural and Food Chemistry, 47, 1208–1216.
Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology, 54, 519–546.
Cagnola J I, Ploschuk E, Benech-Arnold T, Finlayson S A, Casal J J. 2012. Stem transcriptome reveals mechanisms to reduce the energetic cost of shade-avoidance responses in tomato. Plant Physiology, 160, 1110.
Campbell P, Braam J. 1999. Xyloglucan endotransglycosylases: diversity of genes, enzymes and potential wall-modifying functions. Trends in Plant Science, 4, 361–366.
Casal J J. 2012. Shade avoidance. The Arabidopsis Book, 10, e0157.
Choi D, Kim J H, Lee Y. 2008. Expansins in plant development. Advances in Botanical Research, 47, 47–97.
Cosgrove D J. 2000. Loosening of plant cell walls by expansins. Nature, 407, 321–326.
Du J, Han T, Gai J, Yong T, Sun X, Wang X, Yang F, Liu J, Shu K, Liu W, Yang W. 2018. Maize-soybean strip intercropping: Achieved a balance between high productivity and sustainability. Journal of Integrative Agriculture, 17, 747–754.
Fan S, Zhang D, Lei C, Chen H, Xing L, Ma J, Zhao C, Han M. 2016. Proteome analyses using iTRAQ labeling reveal critical mechanisms in alternate bearing Malus prunifolia. Journal of Proteome Research, 15, 3602–3616.
Franklin K A, Whitelam G C. 2005. Phytochromes and shade-avoidance responses in plants. Annals of Botany, 96, 169–175.
Gelderen K, Kang C, Paalman R, Keuskamp D, Hayes S, Pierik R. 2018. Far-red light detection in the shoot regulates lateral root development through the HY5 transcription factor. The Plant Cell, 30, 101–116.
Gommers C M, Visser E J, St Onge K R, Voesenek L A, Pierik R. 2013. Shade tolerance: When growing tall is not an option. Trends in Plant Science, 18, 65.
Gong W, Qi P, Du J, Sun X, Wu X, Song C, Liu W, Wu Y, Yu X, Yong T, Wang X, Yang F, Yan Y, Yang W. 2014. Transcriptome analysis of shade-induced inhibition on leaf size in relay intercropped soybean. PLoS ONE, 9, e98465.
Haigler C H, Ivanova-Datcheva M, Hogan P S, Salnikov V V, Hwang S, Martin K, Delmer D P. 2001. Carbon partitioning to cellulose synthesis. Plant Molecular Biology, 47, 29–51.
Jian W, Zhu J, Lin Q, Li X, Teng N, Li Z, Li B, Zhang A, Lin J. 2006. Effects of stem structure and cell wall components on bending strength in wheat. Chinese Science Bullitin, 51, 815–823.
Johansen D A. 1940. Plant Microtechnique. McGraw-Hill Book Co., New York.
Kashiwagi T, Ishimaru K. 2004. Identification and functional analysis of a locus for improvement of lodging resistance in rice. Plant Physiology, 134, 676–683.
Lee K J D, Marcus S E, Knox J P. 2011. Cell wall biology: Perspectives from cell wall imaging. Molecular Plant, 4, 212–219.
Liu W, Deng Y, Hussaina S, Zou J, Yuan J, Luo L, Yang C, Yuan X, Yang W. 2016. Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean [Glycine max (L.) Merr.)]. Field Crops Research, 196, 261–267.
Liu W, Ren M, Liu T, Du Y, Zhou T, Liu X, Liu J, Hussain S, Yang W. 2018. Effect of shade stress on lignin biosynthesis in soybean stems. Journal of Integrative Agriculture, 17, 1594–1604.
Liu W, Zou J, Zhang J, Yang F, Wang Y, Yang W. 2015. Evaluation of soybean (Glycine max) stem vining in maize-soybean relay strip intercropping system. Plant Production Science, 18, 69–75.
Luo L, Yu X B, Wan Y, Jiang T, Du J B, Zou J, Yang W, Liu W. 2015. The relationship between lodging and stem endogenous gibberellins metabolism pathway of relay intercropping soybean at seedling stage. Scientia Agricultura Sinica, 48, 2528–2537. (in Chinese)
Ma Q. 2009. The expression of caffeic acid 3-O-methyltransferase in two wheat genotypes differing in lodging resistance. Journal of Experimental Botany, 60, 2763–2771.
Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Rapidel B, Tourdonnet S, Valantin-Morison M. 2009. Mixing plant species in cropping systems: Concepts, tools and models. Agronomy for Sustainable Development, 29, 43–62.
Morelli G, Ruberti I. 2002. Light and shade in the photocontrol of Arabidopsis growth. Trends in Plant Science, 7, 399–404.
Paul Francis D, Marcelo Javier Y, Kay S A. 2003. A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiology, 133, 1617–1629.
Ren S, Deng Y, Wen F, Liu M, Yuan X, Pu Q, Liu W, Yang W. 2018. Effects of intercropping on the metabolism of carbon and nitrogen of soybean at the seedling stage and its relationship with lodging. Acta Prataculturae Sinica, 27, 85–94. (in Chinese)
Ross P, Huang Y, Marchese J, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin D. 2004. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Molecular & Cellular Proteomics, 3, 1154–1169.
Sasidharan R, Chinnappa C C, Voesenek L A C J, Pierik R. 2008. The regulation of cell wall extensibility during shade avoidance: A study using two contrasting ecotypes of Stellaria longipes. Plant Physiology, 148, 1557–1569.
Smith H. 1982. Light quality, photoperception, and plant strategy. Annual Review of Plant Physiology, 33, 481–518.
Stitt M, Lilley R M, Gerhardt R, Heldt H W. 1989. Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Methods in Enzymology, 174, 518–552.
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. 2010. Lignin biosynthesis and structure. Plant Physiology, 153, 895–905.
Yang F, Huang S, Gao R, Liu W, Yong T, Wang X, Wu X, Yang W. 2014. Growth of soybean seedlings in relay strip intercropping systems in relation to light quantity and red:far-red ratio. Field Crops Research, 155, 245–253.
Yang L, Qi Y, Lu Y, Guo P, Sang W, Feng H, Zhang H, Chen L. 2013. iTRAQ protein profile analysis of Citrus sinensis roots in response to long-term boron-deficiency. Journal of Proteomics, 93, 179–206.
Zeng J, He X, Quan X, Cai S, Han Y, Nadira U, Zhang G. 2015. Identification of the proteins associated with low potassium tolerance in cultivated and tibetan wild barley. Journal of Proteomics, 126, 1–11.
Zhong R, Ripperger A, Ye Z. 2000. Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiology, 123, 59–70.
Zou J, Liu W, Yuan J, Jiang T, Ye S, Deng Y, Yang C, Yang W. 2015. Relationship between lignin synthesis and lodging resistance at seedlings stage in soybean intercropping system. Acta Agronomica Sinica, 41, 1098–1104. (in Chinese)
[1] YANG Hong-jun, YE Wen-wu, YU Ze, SHEN Wei-liang, LI Su-zhen, WANG Xing, CHEN Jia-jia, WANG Yuan-chao, ZHENG Xiao-bo. Host niche, genotype, and field location shape the diversity and composition of the soybean microbiome[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2412-2425.
[2] XU Lei, ZHAO Tong-hua, Xing Xing, XU Guo-qing, XU Biao, ZHAO Ji-qiu.

Model fitting of the seasonal population dynamics of the soybean aphid, Aphis glycines Matsumura, in the field [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1797-1808.

[3] GAO Hua-wei, YANG Meng-yuan, YAN Long, HU Xian-zhong, HONG Hui-long, ZHANG Xiang, SUN Ru-jian, WANG Hao-rang, WANG Xiao-bo, LIU Li-ke, ZHANG Shu-zhen, QIU Li-juan. Identification of tolerance to high density and lodging in short petiolate germplasm M657 and the effect of density on yield-related phenotypes of soybean[J]. >Journal of Integrative Agriculture, 2023, 22(2): 434-446.
[4] QU Zheng, LI Yue-han, XU Wei-hui, CHEN Wen-jing, HU Yun-long, WANG Zhi-gang. Different genotypes regulate the microbial community structure in the soybean rhizosphere[J]. >Journal of Integrative Agriculture, 2023, 22(2): 585-597.
[5] GAO Hua-wei, SUN Ru-jian, YANG Meng-yuan, YAN Long, HU Xian-zhong, FU Guang-hui, HONG Hui-long, GUO Bing-fu, ZHANG Xiang, LIU Li-ke, ZHANG Shu-zhen, QIU Li-juan. Characterization of the petiole length in soybean compact architecture mutant M657 and the breeding of new lines[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2508-2520.
[6] ZHANG Hua, WU Hai-yan, TIAN Rui, KONG You-bin, CHU Jia-hao, XING Xin-zhu, DU Hui, JIN Yuan, LI Xi-huan, ZHANG Cai-ying. Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of phosphorus utilization in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(9): 2521-2537.
[7] ZOU Jia-nan, ZHANG Zhan-guo, KANG Qing-lin, YU Si-yang, WANG Jie-qi, CHEN Lin, LIU Yan-ru, MA Chao, ZHU Rong-sheng, ZHU Yong-xu, DONG Xiao-hui, JIANG Hong-wei, WU Xiao-xia, WANG Nan-nan, HU Zhen-bang, QI Zhao-ming, LIU Chun-yan, CHEN Qing-shan, XIN Da-wei, WANG Jin-hui. Characterization of chromosome segment substitution lines reveals candidate genes associated with the nodule number in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2197-2210.
[8] PAN Wen-jing, HAN Xue, HUANG Shi-yu, YU Jing-yao, ZHAO Ying, QU Ke-xin, ZHANG Ze-xin, YIN Zhen-gong, QI Hui-dong, YU Guo-long, ZHANG Yong, XIN Da-wei, ZHU Rong-sheng, LIU Chun-yan, WU Xiao-xia, JIANG Hong-wei, HU Zhen-bang, ZUO Yu-hu, CHEN Qing-shan, QI Zhao-ming. Identification of candidate genes related to soluble sugar contents in soybean seeds using multiple genetic analyses[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1886-1902.
[9] LIU Chen, TIAN Yu, LIU Zhang-xiong, GU Yong-zhe, ZHANG Bo, LI Ying-hui, NA Jie, QIU Li-juan. Identification and characterization of long-InDels through whole genome resequencing to facilitate fine-mapping of a QTL for plant height in soybean (Glycine max L. Merr.)[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1903-1912.
[10] HUI Fang, XIE Zi-wen, LI Hai-gang, GUO Yan, LI Bao-guo, LIU Yun-ling, MA Yun-tao. Image-based root phenotyping for field-grown crops: An example under maize/soybean intercropping[J]. >Journal of Integrative Agriculture, 2022, 21(6): 1606-1619.
[11] TIAN Yu, YANG Lei, LU Hong-feng, ZHANG Bo, LI Yan-fei, LIU Chen, GE Tian-li, LIU Yu-lin, HAN Jia-nan, LI Ying-hui, QIU Li-juan. QTL analysis for plant height and fine mapping of two environmentally stable QTLs with major effects in soybean[J]. >Journal of Integrative Agriculture, 2022, 21(4): 933-946.
[12] LIU Sang-lin, CHENG Yan-bo, MA Qi-bin, LI Mu JIANG Ze, XIA Qiu-ju, NIAN Hai. Fine mapping and genetic analysis of resistance genes, Rsc18, against soybean mosaic virus[J]. >Journal of Integrative Agriculture, 2022, 21(3): 644-653.
[13] LIU Li-feng, GAO Le, ZHANG Li-xin, CAI Yu-peng, SONG Wen-wen, CHEN Li, YUAN Shan, WU Ting-ting, JIANG Bing-jun, SUN Shi, WU Cun-xiang, HOU Wen-sheng, HAN Tian-fu. Co-silencing E1 and its homologs in an extremely late-maturing soybean cultivar confers super-early maturity and adaptation to high-latitude short-season regions[J]. >Journal of Integrative Agriculture, 2022, 21(2): 326-335.
[14] OCHAR Kingsley, SU Bo-hong, ZHOU Ming-ming, LIU Zhang-xiong, GAO Hua-wei, SOBHI F. Lamlom, QIU Li-juan. Identification of the genetic locus associated with the crinkled leaf phenotype in a soybean (Glycine max L.) mutant by BSA-Seq technology[J]. >Journal of Integrative Agriculture, 2022, 21(12): 3524-3539.
[15] JIA Jia, WANG Huan, CAI Zhan-dong, WEI Ru-qian, HUANG Jing-hua, XIA Qiu-ju, XIAO Xiao-hui, MA Qi-bin, NIAN Hai, CHENG Yan-bo. Identification and validation of stable and novel quantitative trait loci for pod shattering in soybean [Glycine max (L.) Merr.][J]. >Journal of Integrative Agriculture, 2022, 21(11): 3169-3184.
No Suggested Reading articles found!