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Journal of Integrative Agriculture  2019, Vol. 18 Issue (9): 2029-2040    DOI: 10.1016/S2095-3119(18)62123-9
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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
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Abstract  
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: mssiyangwy@sicau.edu.cn   
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)
 
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