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Journal of Integrative Agriculture  2020, Vol. 19 Issue (11): 2628-2642    DOI: 10.1016/S2095-3119(19)62846-7
Special Issue: 麦类遗传育种合辑Triticeae Crops Genetics · Breeding · Germplasm Resources
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Grain proteomic analysis reveals central stress responsive proteins caused by wheat-Haynaldia villosa 6VS/6AL translocation
ZOU Rong1*, WU Ji-su1*, WANG Ruo-mei1, YAN Yue-ming1, 2  
1 College of Life Science, Capital Normal University, Beijing 100048, P.R.China
2 Hubei Collaborative Innovation Center for Grain Industry (HCICGI), Yangtze University, Jingzhou 434023, P.R.China
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Abstract  Haynaldia villosa (2n=14, VV), a wild grass of the subtribe Triticeae, serves as potential gene resources for wheat genetic improvement.  In this study, the proteome characterization during grain development of Yangmai 5 and Yangmai 5-H. villosa 6VS/6AL translocation line was investigated by a comparative proteomic approach.  Two-dimensional electrophoresis identified 81 differentially accumulated proteins (DAPs) during five grain developmental stages in wheat-H. villosa translocation line.  These proteins were mainly involved in stress defense, storage protein, energy metabolism, protein metabolism and folding, carbon metabolism, nitrogen metabolism, and starch metabolism.  In particular, 6VS/6AL translocation led to significant upregulation of 36 DAPs and specific expression of 11 DAPs such as chitinase, thaumatin-like proteins, glutathione transferase, α-amylase inhibitor, heat shock proteins, and betaine aldehyde dehydrogenase.  These proteins mainly involved in biotic and abiotic stress responses.  Further analysis found that the upstream 1 500 promoter regions of these stress-responsive DAP genes contained multiple high-frequency cis-acting elements related to stress defense such as abscisic acid response element ABRE, methyl jasmonate (MeJA)-response element TGACG-motif and CGTCA-motif involved in oxidative stress and antioxidant response element (ARE).  RNA-seq and RT-qPCR analyses revealed the high expression of these stress-defensive DAP genes in the developing grains, particularly at the early-middle grain filling stages.  Our results demonstrated that 6VS chromosome of H. villosa contains abundant stress-defensive proteins that have potential values for wheat genetic improvement.
Keywords:  6VS/6AL translocation        grain development        proteome        DAPs       cis-acting elements        adverse defense  
Received: 30 July 2019   Accepted:
Fund: This research was financially supported by the National Key R&D Program of China (2016YFD0100502) and the National Natural Science Foundation of China (31771773).
Corresponding Authors:  Correspondence YAN Yue-ming, Tel/Fax: +86-10-68902777, E-mail: yanym@cnu.edu.cn    
About author:  * These authors contributed equally to this study.

Cite this article: 

ZOU Rong, WU Ji-su, WANG Ruo-mei, YAN Yue-ming. 2020. Grain proteomic analysis reveals central stress responsive proteins caused by wheat-Haynaldia villosa 6VS/6AL translocation. Journal of Integrative Agriculture, 19(11): 2628-2642.

Ashraf M, Foolad M. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59, 206–216.
Bagatharia S B, Chanda S V. 1998. Changes in peroxidase and IAA oxidase activities during cell elongation in Phaseolus hypocotyls. Acta Physiologiae Plantarum, 20, 9–13.
Bartling D, Radzio R, Steiner U, Weiler E W. 1993. A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. European Journal of Biochemistry, 216, 579–586.
Bian Y W, Deng X, Yan X, Zhou J X, Yuan L L, Yan Y M. 2017. Integrated proteomic analysis of Brachypodium distachyon roots and leaves reveals a synergistic network in the response to drought stress and recovery. Scientific Reports, 7, 46183.
Bliffeld M, Mundy J, Potrykus I, Futterer J. 1999. Genetic engineering of wheat for increased resistance to powdery mildew disease. Theoretical and Applied Genetics, 98, 1079–1086.
Chen P D, Qi L L, Zhou B, Zhang S Z, Liu D J. 1995. Development and molecular cytogenetic analysis of wheat-H. villosa 6VS/6AI translocation lines specifying resistance to powdery mildew. Theoretical and Applied Genetics, 91, 1125–1128.
Chen T, Murata N. 2002. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Current Opinion in Plant Biology, 5, 250–257.
Chun J, Yu X, Griffith M. 1998. Genetic studies of antifreeze proteins and their correlation with winter survival in wheat. Euphytica, 102, 219–226.
Cochrane M P, Paterson L, Gould E. 2000. Changes in chalazal cell walls and in the peroxidase enzymes of the crease region during grain development in barley. Journal of Experimental Botany, 51, 507–520.
Deng X, Liu Y, Xu X X, Liu D M, Zhu G R, Yan X, Wang Z M, Yan Y M. 2018. Comparative proteome analysis of wheat flag leaves and developing grains under water deficit. Frontiers in Plant Science, 9, 425.
Dong M, Gu J, Zhang L, Chen P, Liu T, Deng J, Lu H, Han L, Zhao B. 2014. Comparative proteomics analysis of superior and inferior spikelets in hybrid rice during grain filling and response of inferior spikelets to drought stress using isobaric tags for relative and absolute quantification. Journal of Proteomics, 109, 382–399.
Dzaman S S, Telatyńska M B, Ciechanowski K. 2005. Heat shock proteins and their characteristics. Polski Merkuriusz Lekarski, 19, 215–219.
Eisen M B, Spellman P T, Brown P O, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proceedings of the National Academy of Sciences of the United States of America, 95, 14863–14868.
Fang Y, Liu Y, Wu H, Zhang Q, Chen P, Liu D. 2000. Construction of a transformation-competent artificial chromosome (TAC) library of a wheat-H. villosa translocation line. Chinese Jounal of Biotechnology, 16, 433–436.
Finnie C, Melchior S, Roepstorff P, Svensson B. 2002. Proteome analysis of grain filling and seed maturation in barley. Plant Physiology, 129, 1308–1319.
Octávio L F, Daniel J R, Francislete R M, Maria F G. 2002. Plant alpha-amylase inhibitors and their interaction with insect alpha-amylases. European Journal of Biochemistry, 269, 397–412.
Gao L, Wang A, Li X, Dong K, Wang K, Appels R, Ma W, Yan Y. 2009. Wheat quality related differential expressions of albumins and globulins revealed by two-dimensional difference gel electrophoresis (2-D DIGE). Journal of Proteomics, 73, 279–296.
Gao L, Yan X, Li X, Guo G F, Hu Y K, Ma W J, Yan Y M. 2011. Proteome analysis of wheat leaf under salt stress by two-dimensional difference gel electrophoresis (2D-DIGE). Phytochemistry, 72, 1180–1191.
Ge P, Ma C, Wang S, Gao L, Li X, Guo G. 2012. Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Analytical and Bioanalytical Chemistry, 402, 1297–1313.
Gu A Q, Hao P C, Lv D W, Zhen S M, Bian Y W, Ma C Y, Li X H, Zhang W Y, Yan Y M. 2015. Integrated proteome analysis of the wheat embryo and endosperm reveals central metabolic changes involved in water deficit response during the grain development. Journal of Agricultural and Food Chemistry, 63, 8478–8487.
Guillon F, Larré C, Petipas F, Berger A, Moussawi J, Rogniaux H, Santoni A, Saulnier L, Jamme F, Miquel M, Lepiniec L, Dubreucq B. 2012. A comprehensive overview of grain development in Brachypodium distachyon variety Bd21. Journal of Experimental Botany, 63, 739–755.
Guo G F, Lv D W, Yan X, Subburaj S, Ge P, Li X, Hu Y K, Yan Y M. 2012. Proteome characterization of developing grains in bread wheat cultivars (Triticum aestivum L.). BMC Plant Biology, 12, 147.
He D L, Han C, Yao J L, Shen S H, Yang P F. 2011. Constructing the metabolic and regulatory pathways in germinating rice seeds through proteomic approach. Proteomics, 11, 2693–2713.
He H, Zhu S, Wang X, Chen P. 2008. Cloning and sequence analysis of a cyclophilin gene from wheat-H. villosa 6VS/6AL translocation line. Jounal of Henan Agricultural Sciences, 1, 12. (in Chinese)
He M, Zhu C, Dong K, Zhang T, Cheng Z W, Li J R, Yan Y M. 2015. Comparative proteome analysis of embryo and endosperm reveals central differential expression proteins involved in wheat seed germination. BMC Plant Biology, 15, 97.
Horton P, Park K J, Obayashi T, Nakai K. 2006. Protein subcellular localization prediction with WOLF PSORT. Nucleic Acids Research, 3, 39–48.
Huang Y, Xiao B, Xiong L. 2007. Characterization of a stress responsive proteinase inhibitor gene with positive effect in improving drought resistance in rice. Planta, 226, 73–85.
Jiang C, Cheng Z, Zhang C, Yu T, Zhong Q, Shen J Q, Huang X. 2014. Proteomic analysis of seed storage proteins in wild rice species of the Oryza genus. Proteome Science, 12, 51.
Jiang S S, Liang X N, Li X, Wang S L, Lv D W, Ma C Y. 2012. Wheat drought-responsive grain proteome analysis by linear and nonlinear 2-DE and MALDI-TOF mass spectrometry. International Journal of Molecular Sciences, 13, 16065–16083.
Johansson E, Prieto-Linde M L, Jönsson J Ö. 2001. Effects of wheat cultivar and nitrogen application on storage protein composition and breadmaking quality. Cereal Chemistry, 78, 685.
Kaur S, Dhugga K S, Beech R, Singh J. 2017. Genome-wide analysis of the cellulose synthase-like (Csl) gene family in bread wheat (Triticum aestivum L.). BMC Plant Biology, 17, 193.
Kumar S, Asif M H, Chakrabarty D, Tripathia R D, Dubeyb R S, Trivedi P K. 2013. Expression of a rice lambda class of glutathione S-transferase, OsGSTL2, in Arabidopsis provides tolerance to heavy metal and other abiotic stresses. Journal of Hazardous Materials, 248, 228–237.
Kumar S, Dhingra A, Daniell H. 2004. Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiology, 136, 2843–2854.
Li C, Huang H, Yin F, Wang Z, Peng Y, Xie C, Liu Z, Sun Q, Yang Z. 2008. The effect of H. villosa V chromosome on the mitochonarial proteome of wheat-H. villosa chromosome substitution line and translocation line. Journal of Molecular Cell Biology, 41, 150–154.
Li H, Chen X, Xin Z, Xu H. 2008. Development and identification of wheat-H. villosa T6DL.6VS chromosome translocation lines conferring resistance to powdery mildew. Plant Breeding, 124, 203–205.
Liu D J, Chert P D, Pei G Z, Wang Y N, Qiu B X, Wang S L. 1983. Studies on transfer of genetic material from H. villosa to Triticum aestivum L. Acta Genetica Sinica, 2, 355–361.
Liu J J, Sturrock R, Ekramoddoullah A K. 2010. The superfamily of thaumatin-like proteins: Its origin, evolution, and expression towards biological function. Plant Cell Reports, 29, 419–436.
Liu Y, Wang S, Wang C, Chen G, Cao H, Wang Y, Ma W, Hu Y, Yan Y. 2016. Comparative proteomic analysis of wheat developing grains between Chinese Spring and 1Sl/1B substitution line. Cereal Research Communications, 44, 13–23.
Liu Z, Sun Q, Ni Z, Yang T. 1999. Development of SCAR markers linked to the Pm21 gene conferring resistance to powdery mildew in common wheat. Plant Breeding, 118, 215–219.
Luo D, Niu X, Yu J, Yan J, Gou X, Lu B R, Liu Y S. 2012. Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). Plant Cell Reports, 31, 1625–1635.
Lv D W, Subburaj S, Cao M, Yan X, Li X, Appels R, Sun D, Ma W J, Yan Y M. 2014. Proteome and phosphoproteome characterization reveals new response and defense mechanisms of Brachypodium distachyon leaves under salt stress. Molecular and Cellular Proteomics, 13, 632–652.
Lv D W, Zhu G R, Zhu D, Bian Y W, Liang X N, Cheng Z W, Deng X, Yan Y M. 2016. Proteomic and phosphoproteomic analysis reveals the response and defense mechanism in leaves of diploid wheat T. monococcum under salt stress and recovery. Journal of Proteomics, 143, 93–105.
Marjamaa K, Kukkola E, Lundell T, Karhunen P, Saranpaa P, Fagerstedt K V. 2006. Monolignol oxidation by xylem peroxidase isoforms of Norway spruce (Picea abies) and silver birch (Betula pendula). Tree Physiology, 26, 605–611.
Misra R C, Sandeep, Kamthan M, Kumar S, Ghosh S. 2016. A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Scientific Reports, 6, 25340.
Niu X, Zheng W, Lu B R, Ren G, Huang W, Wang S, Liu J, Tang Z, Luo D, Wang Y, Liu Y. 2007. An unusual posttranscriptional processing in two betaine aldehyde dehydrogenase loci of cereal crops directed by short, direct repeats in response to stress conditions. Plant Physiology, 143, 1929–1942.
Oldach K H, Becker D, Lorz H. 2001. Heterologous expression of genes mediating enhanced fungal resistance in transgenic wheat. Molecular Plant Microbe Interactions, 14, 832–838.
Orozco-Cárdenas M L, Narváez-Vásquez J, Ryan C A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. The Plant Cell, 13, 179–191.
Park C J, Seo Y S. 2015. Heat shock proteins: A review of the molecular chaperones for plant immunity. The Plant Pathology Journal, 31, 323–333.
Petre B, Major I, Rouhier N, Duplessis S. 2011. Genome-wide analysis of eukaryote thaumatin-like proteins (TLPs) with an emphasis on poplar. BMC Plant Biology, 11, 33.
Qi L L, Chert P D, Liu D J. 1995. The gene Pm21-a new source of resistance to wheat powdery mildew. Acta Agronomica Sinica, 21, 257–260. (in Chinese)
Shan Q W, Wang Y P, Li J, Gao C X. 2014. Genome editing in rice and wheat using the CRISPR/Cas system. Nature Protocol, 9, 2395–2410.
Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K. 2002. Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53, 1305–1319.
Shin S, Mackintosh C A, Lewis J, Heinen S J, Radmer L, Dill-Macky R, Baldridge G D, Zeyen R J, Muehlbauer G J. 2008. Transgenic wheat expressing a barley class II chitinase gene has enhanced resistance against Fusarium graminearum. Journal of Experimental Botany, 59, 2371–2378.
Singha S, Tripathia R K, Lemauxb P G, Buchananb B B, Singha J. 2017. Redox-dependent interaction between thaumatin-like protein and β-glucan influences malting quality of barley. Proceedings of the National Academy of Sciences of the United States of America, 29, 7725–7730.
Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics, 4, 1581–1590.
Toyoda H, Matsuda Y, Yamaga T, Ikeda S, Morita M, Tamai T, Ouchi S. 1991. Suppression of the powdery mildew pathogen by chitinase microinjected into barley coleoptile epidermal cells. Plant Cell Reports, 10, 217–220.
Truyen N, Philip J S, Cecil B P. 2003. Regulatory mechanisms controlling gene mediated by the antioxidant response element. Annual Review of Pharmacology and Toxicology, 43, 233–260.
Vensel W H, Tanaka C K, Cai N, Wong J H, Buchanan B B, Hurkman W J. 2005. Developmental changes in the metabolic protein profiles of wheat endosperm. Proteomics, 5, 1594–1611.
Wan Y, Poole R L, Huttly A K, Toscano-Underwood C, Feeney K, Welham S, Gooding M J, Mills C, Edwards K J, Shewry P R. 2008. Transcriptome analysis of grain development in hexaploid wheat. BMC Genomics, 9, 121.
Wang R M, Wu J S, Deng X, Liu D M, Yan Y M. 2018. Drought-responsive protein identification in developing grains of a wheat-H. villosa 6VS/6AL translocation line. Crop & Pasture Science, 69, 1182–1196.
Weretilnyk E A, Hanson A D. 1990. Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proceedings of the National Academy of Sciences of the United States of America, 87, 2745–2749.
Yang F, Jørgensen A D, Li H, Søndergaard I, Finnie C, Svensson B, Jiang D, Wollenweber B, Jacobsen S. 2011. Implications of high-temperature events and water deficits on protein profiles in wheat (Triticum aestivum L. cv. Vinjett) grain. Proteomics, 11, 1684–1695.
Yang P, Li X, Wang X, Chen H, Chen F, Shen S. 2007. Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics, 7, 3358–3368.
Yu J, Li Y, Tang W, Liu J, Lu B R, Liu Y. 2014. The accumulation of glycine betaine is dependent on choline monooxygenase (OsCMO), not on phosphoethanolamine N-methyltransferase (OsPEAMT1), in rice (Oryza sativa L. ssp. japonica). Plant Molecular Biology Reporter, 36, 916–922.
Yu Y L, Zhu D, Ma C Y, Cao H, Wang Y P, Xu Y H, Zhang W Y, Yan Y M. 2016. Transcriptome analysis reveals key differentially expressed genes involved in wheat grain development. The Crop Journal, 4, 92–106.
Zhang W, Zhang R Q, Feng Y G, Bie T D, Chen P D. 2013. Distribution of highly repeated DNA sequences in H. villosa and its application in the identification of alien chromatin. Chinese Science Bulletin, 8, 890–897.
Zhou J X, Ma C Y, Zhen S M, Cao M, Zeller F J, Hsam S K, Yan Y M. 2016. Identification of drought stress related proteins from 1Sl(1B) chromosome substitution line of wheat variety Chinese Spring, Botanic Studies, 57, 20.
Zhu B, Chen T, Li P. 1996. Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for osmotin-like protein. Planta, 198, 70–77.
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