Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize

doi:10.1016/S2095-3119(13)60513-4

Journal of Integrative Agriculture ›› 2014, Vol. 13 ›› Issue (4): 789-803.DOI: 10.1016/S2095-3119(13)60513-4

Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize

ZHANG Xiao-li, SI Bing-wen, FAN Cheng-ming, LI Hong-jie , WANG Xiao-ming

1、Institute of Crop Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2、Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
3、Beijing Plant Protection Station, Beijing 100029, P.R.China

收稿日期:2013-02-18 出版日期:2014-04-01 发布日期:2014-04-16
通讯作者: WANG Xiao-ming, Tel: +86-10-82109609, Fax: +86-10-82109608, E-mail: wangxiaoming@caas.cn
作者简介:ZHANG Xiao-li, E-mail: comeonzxl@126.com
基金资助:
This work was supported by the China Agriculture Research System (Maize) (CARS-02).

Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize

ZHANG Xiao-li, SI Bing-wen, FAN Cheng-ming, LI Hong-jie , WANG Xiao-ming

1、Institute of Crop Sciences/National Key Facility for Crop Gene Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2、Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
3、Beijing Plant Protection Station, Beijing 100029, P.R.China

Received:2013-02-18 Online:2014-04-01 Published:2014-04-16
Contact: WANG Xiao-ming, Tel: +86-10-82109609, Fax: +86-10-82109608, E-mail: wangxiaoming@caas.cn
About author:ZHANG Xiao-li, E-mail: comeonzxl@126.com
Supported by:
This work was supported by the China Agriculture Research System (Maize) (CARS-02).

摘要/Abstract

摘要： Northern corn leaf blight (NCLB), caused by the heterothallic ascomycete fungus Setosphaeria turcica, is a destructive foliar disease of maize and represents a serious threat to maize production worldwide. A comparative proteomic study was conducted to explore the molecular mechanisms underlying the defense responses of the maize resistant line A619 Ht2 to S. turcica race 13. Leaf proteins were extracted from mock and S. turcica-infected leaves after inoculated for 72 h and analyzed for differentially expressed proteins using two-dimensional electrophoresis and mass spectrometry identification. 137 proteins showed reproducible differences in abundance by more than 2-fold at least, including 50 up-regulated proteins and 87 down-regulated proteins. 48 protein spots were successfully identified by MS analysis, which included 10 unique, 6 up-regulated, 20 down-regulated and 12 disappeared protein spots. These identified proteins were classified into 9 functional groups and involved in multiple functions, particularly in energy metabolism (46%), protein destination and storage (12%), and disease defense (18%). Some defense-related proteins were upregulated such as β-glucosidase, SOD, polyamines oxidase, HSC 70 and PPIases; while the expressions of photosynthesis- and metabolism-related proteins were down-regulated, by inoculation with S. turcica. The results indicated that a complex regulatory network was functioned in interaction between the resistant line A619 Ht2 and S. turcica. The resistance processes of A619 Ht2 mainly resided on directly releasing defense proteins, modulation of primary metabolism, affecting photosyntesis and carbohydrate metabolism.

关键词: maize , Setosphaeria turcica , Ht2 gene , differential proteomics

Abstract: Northern corn leaf blight (NCLB), caused by the heterothallic ascomycete fungus Setosphaeria turcica, is a destructive foliar disease of maize and represents a serious threat to maize production worldwide. A comparative proteomic study was conducted to explore the molecular mechanisms underlying the defense responses of the maize resistant line A619 Ht2 to S. turcica race 13. Leaf proteins were extracted from mock and S. turcica-infected leaves after inoculated for 72 h and analyzed for differentially expressed proteins using two-dimensional electrophoresis and mass spectrometry identification. 137 proteins showed reproducible differences in abundance by more than 2-fold at least, including 50 up-regulated proteins and 87 down-regulated proteins. 48 protein spots were successfully identified by MS analysis, which included 10 unique, 6 up-regulated, 20 down-regulated and 12 disappeared protein spots. These identified proteins were classified into 9 functional groups and involved in multiple functions, particularly in energy metabolism (46%), protein destination and storage (12%), and disease defense (18%). Some defense-related proteins were upregulated such as β-glucosidase, SOD, polyamines oxidase, HSC 70 and PPIases; while the expressions of photosynthesis- and metabolism-related proteins were down-regulated, by inoculation with S. turcica. The results indicated that a complex regulatory network was functioned in interaction between the resistant line A619 Ht2 and S. turcica. The resistance processes of A619 Ht2 mainly resided on directly releasing defense proteins, modulation of primary metabolism, affecting photosyntesis and carbohydrate metabolism.

Key words: maize , Setosphaeria turcica , Ht2 gene , differential proteomics

ZHANG Xiao-li, SI Bing-wen, FAN Cheng-ming, LI Hong-jie , WANG Xiao-ming. Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize[J]. Journal of Integrative Agriculture, 2014, 13(4): 789-803.

参考文献

Acharya K, Pal A K, Gulati A, Kumar S, Singh A K, Ahuja P S. 2012. Overexpression of Camellia sinensis thaumatin-like protein, CsTLP in potato confers enhanced resistance to Macrophomina phaseolina and Phytophthora infestans infection. Molecular Biotechnology, 54, 1-14

Adam A, Jourdan E, Ongena M, Duby F, Dommes J, Thonart P. 2005. Resistance induced in cucumber and tomato by a non-pathogenic Pseudomonas putida strain. Parasitica, 61, 13-22

Adamiec M, Drath M, Jackowski G. 2008. Redox state of plastoquionone pool regulates expression of Arabidopsis thaliana genes in response to elevated irradiance. Acta Biochimica Polonica-English Edition, 55, 161-173

Ahn I P, Kim S, Lee Y H. 2005. Vitamin B1 functions as an activator of plant disease resistance. Plant Physiology, 138, 1505-1515

Alvarado V Y, Odokonyero D, Duncan O, Mirkov T E, Scholthof H B. 2012. Molecular and physiological properties associated with zebra complex disease in potatoes and its relation with Candidatus Liberibacter contents in psyllid vectors. PloS One, 7, e37345.

Angelova S, Buchheim M, Frowitter D, Schierhorn A, Roos W. 2010. Overproduction of alkaloid phytoalexins in California poppy cells is associated with the co- expression of biosynthetic and stress-protective enzymes. Molecular Plant, 3, 927-939

Asano T, Kimura M, Nishiuchi T. 2012. The defense response in Arabidopsis thaliana against Fusarium sporotrichioides. Proteome Science, 10, 61-70

Batchvarova R, Reddy V, Bennett J. 1992. Cellular resistance in rice to cercosporin, a toxin of Cercospora. Phytopathology, 82, 642-646

Bentolila S, Guitton C, Bouvet N, Sailland A, Nykaza S, Freyssinet G. 1991. Identification of an RFLP marker tightly linked to the Ht1 gene in maize. Theoretical and Applied Genetics, 82, 393-398

Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, van Staveren M, Stiekema W. 1998. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature, 391, 485-488

Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254

van Breusegem F, Dat J F. 2006. Reactive oxygen species in plant cell death. Plant Physiology, 141, 384-390

Carson M. 1995a. A new gene in maize conferring the “chlorotic halo” reaction to infection by Exserohilum turcicum. Plant Disease, 79, 717-720

Carson M. 1995b. Inheritance of latent period length in maize infected with Exserohilum turcicum. Plant Disease, 79, 581-585

Chen Z Y, Brown R, Damann K, Cleveland T. 2007. Identification of maize kernel endosperm proteins associated with resistance to aflatoxin contamination by Aspergillus flavus. Phytopathology, 97, 1094-1103

Cheng P, Wang X, Gao W. 2007. Practical detection of molecular markers for resistance gene Ht2, Ht3 to northern corn leaf blight. Journal of Plant Genetic Resources, 8, 285-288 (in Chinese)

Chiang M, van Dyke C, Leonard K. 1989. Evaluation of endemic foliar fungi for potential biological control of johnsongrass (Sorghum halepense): Screening and host range tests. Plant Disease, 73, 459-464

Chisholm S T, Coaker G, Day B, Staskawicz B J. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124, 803-814

Chivasa S, Tomé D F A, Hamilton J M, Slabas A R. 2011. Proteomic analysis of extracellular ATP-regulated proteins identifies ATP synthase β-subunit as a novel plant cell death regulator. Molecular and Cellular Proteomics, 10, 1-13

Chung C L, Jamann T, Longfellow J, Nelson R. 2010. Characterization and fine-mapping of a resistance locus for northern leaf blight in maize bin 8.06. Theoretical and Applied Genetics, 121, 205-227

Cona A, Rea G, Botta M, Corelli F, Federico R, Angelini R. 2006. Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. Journal of Experimental Botany, 57, 2277-2289

Cooper B, Campbell K B, Feng J, Garrett W M, Frederick R. 2011. Nuclear proteomic changes linked to soybean rust resistance. Molecular BioSystems, 7, 773-783

Dahal D, Pich A, Braun H P, Wydra K. 2010. Analysis of cell wall proteins regulated in stem of susceptible and resistant tomato species after inoculation with Ralstonia solanacearum: A proteomic approach. Plant Molecular Biology, 73, 643-658

Day B, Henty J L, Porter K J, Staiger C J. 2011. The pathogen-actin connection: A platform for defense signaling in plants. Annual Review of Phytopathology, 49, 483-506

Dick R, Rattei T, Haslbeck M, Schwab W, Gierl A, Frey M. 2012. Comparative analysis of benzoxazinoid biosynthesis in monocots and dicots: independent recruitment of stabilization and activation functions. The Plant Cell, 24, 915-928

Duressa D, Soliman K, Taylor R, Senwo Z. 2011. Proteomic analysis of soybean roots under aluminum stress. International Journal of Plant Genomics, doi: 10.1155/2011/282531

Edwards G E, Franceschi V R, Voznesenskaya E V. 2004. Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annual Review of Plant Biology, 55, 173-196

Gao X, Brodhagen M, Isakeit T, Brown S H, Göbel C, Betran J, Feussner I, Keller N P, Kolomiets M V. 2009. Inactivation of the lipoxygenase ZmLOX3 increases susceptibility of maize to Aspergillus spp. Molecular Plant-Microbe Interactions, 22, 222-231

Gevers H O. 1975. A new major gene for resistance to Helminthosporium turcicum leaf blight in maize. Plant Disease Reporter, 59, 296-299

H a m i d A B H, Aragaki M. 1975. Inheritance of pathogenicity in Setosphaeria turcica. Phytopathology, 65, 280-283

Heath M C. 2000. Nonhost resistance and nonspecific plant defenses. Current Opinion in Plant Biology, 3, 315-319

Hooker A L. 1963. Inheritance of chlorotic-lesion resistance to Helminthosporium turcicum in seedling corn. Phytopathology, 53, 660-662

Hooker A L. 1977. A second major gene locus in corn for chlorotic-lesion resistance to Helminthosporium turicum. Crop Science, 17, 132-135

Hooker A L. 1981. Resistance to Helminthosporium turcicum from Tripsacum floridanum incorporated into corn. Maize Genetics Cooperation News Letter, 55, 87- 88.

Huang X, Liu L, Chen J, Zhai Y. 2009. Comparative proteomic analysis of the response in resistant and susceptible maize inbred lines to infection by Curvularia lunata. Progress in Natural Science, 19, 845-850

Ishikawa T, Yoshimura K, Tamoi M, Takeda T, Shigeoka S. 1997. Alternative mRNA splicing of 3´-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplasts. Biochemical Journal, 328, 795-800

Jiang Y, Yang B, Harris N S, Deyholos M K. 2007. Comparative proteomic analysis of NaCl stress- responsive proteins in Arabidopsis roots. Journal of Experimental Botany, 58, 3591-3607

Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi R. 2003. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana.Molecular Plant Pathology, 4, 383-391

Kim S K, You Y N, Park J C, Joung Y, Kim B G, Ahn J C,Cho H S. 2012. The rice thylakoid lumenal cyclophilinOsCYP20-2 confers enhanced environmental stress tolerance in tobacco and Arabidopsis

Plant Cell Reports, 31, 417-426

Kirsch R, Vogel H, Muck A, Reichwald K, Pasteels J M,Boland W. 2011. Host plant shifts affect a major defenseenzyme in Chrysomela lapponica. Proceedings of the National Academy of Sciences of the United States of America, 108, 4897-4901

Kobayashi S D, Voyich J M, Burlak C, DeLeo F R. 2005.Neutrophils in the innate immune response. ArchivumImmunologiae et Therapiae Experimentalis, 53, 505-517

Kregel K C. 2002. Heat shock proteins: Modifyingfactors in physiological stress responses and acquiredthermotolerance. Journal of Applied Physiology, 92,2177-2186

Lavy M, Prigge M J, Tigyi K, Estelle M. 2012. The cyclophilin DIAGEOTROPICA has a conserved role inauxin signaling. Development, 139, 1115-1124

Levy Y, Cohen Y. 1983. Biotic and environmental factors affecting infection of sweet corn with Exserohilumturcicum. Phytopathology, 73, 722-725

Li J, Zhao P J, Ma C L, Zeng Y. 2012. A chitosan induced9-lipoxygenase in Adelostemma gracillimum seedlings.International Journal of Molecular Sciences, 13, 540-551

Li K, Xu C, Zhang J. 2011. Proteome profile of maize (Zeamays L.) leaf tissue at the flowering stage after longtermadjustment to rice black-streaked dwarf virus infection.Gene, 485, 106-113

Lin Y H, Huang H E, Chen Y R, Liao P L, Chen C L, FengT Y. 2011. C-terminal region of plant ferredoxin-like protein is required to enhance resistance to bacterial disease in Arabidopsis thaliana. Phytopathology, 101,741-749

Liu Y, Du H, He X, Huang B, Wang Z. 2011. Identificationof differentially expressed salt-responsive proteins in roots of two perennial grass species contrasting insalinity tolerance. Journal of Plant Physiology, 169,117-126

Mahmood T, Jan A, Kakishima M, Komatsu S. 2006.Proteomic analysis of bacterial blight defense responsiveproteins in rice leaf blades. Proteomics, 6, 6053-6065

Martin T, Biruma M, Fridborg I, Okori P, Dixelius C. 2011.A highly conserved NB-LRR encoding gene cluster effective against Setosphaeria turcica in sorghum. BMCPlant Biology, 11, 151.

Mohammadi M, Anoop V, Gleddie S, Harris L J. 2011. Proteomic profiling of two maize inbreds during earlygibberella ear rot infection. Proteomics, 11, 3675-3684

Moschou P N, Sarris P F, Skandalis N, Andriopoulou A H,Paschalidis K A, Panopoulos N J, Roubelakis-AngelakisK A. 2009. Engineered polyamine catabolism preinducestolerance of tobacco to bacteria and oomycetes. Plant Physiology, 149, 1970-1981

M u llineaux P M, Rausch T. 2005. Glutathione,photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research,86, 459-474

Nejat N, Vadamalai G, Dickinson M. 2012. Expressionpatterns of genes involved in the defense and dtress response of Spiroplasma citri infected Madagascar periwinkle Catharanthus roseus. International Journal of Molecular Sciences, 13, 2301-2313

Ogliari J B, Guimarães M A, Camargo L E A. 2007.Chromosomal locations of the maize (Zea mays L.)HtP and rt genes that confer resistance to Exserohilumturcicum. Genetics and Molecular Biology, 30, 630-634

Ogliari J B, Guimarães M A, Geraldi I O, Camargo L E A.2005. New resistance genes in the Zea mays-Exserohilumturcicum pathosystem. Genetics and Molecular Biology,28, 435-439

Pechanova O, Pechan T, Williams W P, Luthe D S. 2011.Proteomic analysis of the maize rachis: Potential roles of constitutive and induced proteins in resistance toAspergillus flavus infection and aflatoxin accumulation.Proteomics, 11, 114-127

Ramathani I, Biruma M, Martin M, Dixelius C, Okori P. 2011. Disease severity, incidence and races of Setosphaeria turcica on sorghum in Uganda. EuropeanJournal of Plant Pathology, 131, 383-392

Rapala-Kozik M, Kowalska E, Ostrowska K. 2008.Modulation of thiamine metabolism in Zea maysseedlings under conditions of abiotic stress. Journal of Experimental Botany, 59, 4133-4143

Robbins W A, Warren H L. 1993. Inheritance of resistanceto Exserohilum turcicum in PI 209135, ‘Mayorbela’ variety of maize. Maydica, 38, 209-213

Ruan S L, Ma H S, Wang S H, Fu Y P, Xin Y, Liu W Z, Wang F, Tong J X, Wang S Z, Chen H Z. 2011.Proteomic identification of OsCYP2, a rice cyclophilinthat confers salt tolerance in rice (Oryza sativa L.)seedlings when overexpressed. BMC Plant Biology, 11,34-48

Schechert A, Welz H, Geiger H. 1999. QTL for resistanceto Setosphaeria turcica in tropical African maize. CropScience, 39, 514-523

Simcox K D, Bennetzen J L. 1993. The use of molecular markers to study Setosphaeria turcica resistance inmaize. Phytopathology, 83, 1326-1330

Sivaguru M, Pike S, Gassmann W, Baskin T I. 2003.Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor.Plant and Cell Physiology, 44, 667-675

Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour A A, Jazii F R, Motamed N, Komatsu S. 2010. Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Science, 8, 19-33

Spasojevi? I, Mojovi? M, Blagojevi? D, Spasi? S D, Jones D R, Nikoli?-Koki? A, Spasi? M B. 2009. Relevance of the capacity of phosphorylated fructose to scavenge the hydroxyl radical. Carbohydrate Research, 344, 80-84

van Staden D, Lambert C A, Lehmensiek A. 2001. SCAR markers for the Ht1, Ht2, Ht3 and Htn1 resistance genes in maize. Maize Genetics Conference Abstract, 43, 134.

V a s a n t h a i a h H K N, Katam R, Basha S M. 2009. Characterization of unique and differentially expressed proteins in anthracnose-tolerant Florida hybrid bunch grapes. Applied Biochemistry and Biotechnology, 157, 395-406

Wang X, Yang P, Zhang X, Xu Y, Kuang T, Shen S, He Y. 2009. Proteomic analysis of the cold stress response in the moss, Physcomitrella patens. Proteomics, 9, 4529- 4538.

Welz H, Geiger H. 2000. Genes for resistance to northern corn leaf blight in diverse maize populations. Plant Breeding, 119, 1-14

Welz H, Xia X, Bassetti P, Melchinger A, Lübberstedt T. 1999. QTLs for resistance to Setosphaeria turcica in an early maturing Dent×Flint maize population. Theoretical and Applied Genetics, 99, 649-655

Xu C, Huang B. 2010. Differential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars differing in stress tolerance. Journal of Plant Physiology, 167, 1477-1485

Xu P, Roes J, Segal A W, Radulovic M. 2006. The role of grancalcin in adhesion of neutrophils. Cellular Immunology, 240, 116-121

Xu Y, Gianfagna T, Huang B. 2010. Proteomic changes associated with expression of a gene (ipt) controlling cytokinin synthesis for improving heat tolerance in a perennial grass species. Journal of Experimental Botany, 61, 3273-3289

Yoda H, Hiroi Y, Sano H. 2006. Polyamine oxidase is one of the key elements for oxidative burst to induce programmed cell death in tobacco cultured cells. Plant Physiology, 142, 193-206

Zhang C, Guy C. 2006. In vitro evidence of Hsc70 functioning as a molecular chaperone during cold stress. Plant Physiology and Biochemistry, 44, 844-850

Zhang M H, Xu X D, Liu K J, Dong H Y, Jiang Y, Hu L. 2011. Physiological differentiation and races distribution of Exserohilum turcicum in China. Journal of Maize Sciences, 19, 138-141 (in Chinese)

Zhang Y M, Zhao J M, Xiang Y, Bian X C, Zuo Q M, Shen Q, Gai J Y, Xing H. 2011. Proteomics study of changes in soybean lines resistant and sensitive to Phytophthora sojae. Proteome Science, 9, 52-64

[1]	. [J]. Journal of Integrative Agriculture, 2022, 21(5): 1253-1265.
[2]	ZHANG Dong-feng, ZHANG Nan, ZHONG Tao, WANG Chao, XU Ming-liang, YE Jian-rong. Identification and characterization of the GH3 gene family in maize[J]. Journal of Integrative Agriculture, 2016, 15(2): 249-261.
[3]	LU Da-lei, YANG Huan, SHEN Xin, LU Wei-ping. Effects of high temperature during grain filling on physicochemical properties of waxy maize starch[J]. Journal of Integrative Agriculture, 2016, 15(2): 309-316.
[4]	SUN Le-xiu, LIU Shuang-xi, WANG Jin-xing, WU Cheng-lai, LI Yan, ZHANG Chun-qing. The effects of grain texture and phenotypic traits on the thin-layer drying rate in maize (Zea mays L.) inbred lines[J]. Journal of Integrative Agriculture, 2016, 15(2): 317-325.
[5]	LI Qi-song, WU Lin-kun, CHEN Jun, Muhammad A Khan, LUO Xiao-mian, LIN Wen-xiong. Biochemical and microbial properties of rhizospheres under maize/ peanut intercropping[J]. Journal of Integrative Agriculture, 2016, 15(1): 101-110.
[6]	ZHANG Su-jiang, Abdul Shakoor Chaudhry, Diky Ramdani, Amerjan Osman, GUO Xue-feng, Grant Raymond Edwards, Long Cheng. Chemical composition and in vitro fermentation characteristics of high sugar forage sorghum as an alternative to forage maize for silage making in Tarim Basin, China[J]. Journal of Integrative Agriculture, 2016, 15(1): 175-182.
[7]	LI Cong-feng, TAO Zhi-qiang, LIU Peng, ZHANG Ji-wang, ZHUANG Ke-zhang, DONG Shu-ting, ZHAO Ming. Increased grain yield with improved photosynthetic characters in modern maize parental lines[J]. Journal of Integrative Agriculture, 2015, 14(9): 1735-1744.
[8]	WANG Zhan-biao, WEN Xin-ya, ZHANG Hai-lin, LU Xiao-hong, CHEN Fu. Net energy yield and carbon footprint of summer corn under different N fertilizer rates in the North China Plain[J]. Journal of Integrative Agriculture, 2015, 14(8): 1534-1541.
[9]	LIANG Ming-yuan, WANG Gui-yan, LIANG Wei-li, SHI Peng-fei, DANG Jing, SUI Peng, HU Chun-sheng. Yield and quality of maize stover: Variation among cultivars and effects of N fertilization[J]. Journal of Integrative Agriculture, 2015, 14(8): 1581-1587.
[10]	CHENG Yi, ZHAO Jie, LIU Zhen-xiang, HUO Zhi-jin, LIU Peng, DONG Shu-ti ng, ZHANG Ji-wang, ZHAO Bin. Modified fertilization management of summer maize (Zea mays L.) in northern China improves grain yield and efficiency of nitrogen use[J]. Journal of Integrative Agriculture, 2015, 14(8): 1644-1657.
[11]	ZHANG Fan, CHEN Xun-ji, WANG Jian-hua, ZHENG Jun. Overexpression of a maize SNF-related protein kinase gene, ZmSnRK2.11, reduces salt and drought tolerance in Arabidopsis[J]. Journal of Integrative Agriculture, 2015, 14(7): 1229-1241.
[12]	K?stutis Romaneckas, Egidijus ?arauskis, Dovil? Avi?ienyt?, Sidona Buragien?, David Arney. The main physical properties of planosol in maize (Zea mays L.) cultivation under different long-term reduced tillage practices in the Baltic region[J]. Journal of Integrative Agriculture, 2015, 14(7): 1309-1320.
[13]	BO Xiao-dong, DU Tai-sheng, DING Ri-sheng, TONG Ling, LI Si-en. Stem flow of seed-maize under alternate furrow irrigation and double-row ridge planting in an arid region of Northwest China[J]. Journal of Integrative Agriculture, 2015, 14(7): 1434-1445.
[14]	ZHOU De, Dieter Koemle. Price transmission in hog and feed markets of China[J]. Journal of Integrative Agriculture, 2015, 14(6): 1122-1129.
[15]	FU Jie, YANG Xiu-yan, CHENG Ming-jun, Lü Gui-hua, WANG Pei, WU Yuan-qi, ZHENG Ming-min, ZHOU Shu-feng, RONG Ting-zhao, TANG Qi-lin. Perennial aneuploidy as a potential material for gene introgression between maize and Zea perennis[J]. Journal of Integrative Agriculture, 2015, 14(5): 839-846.

Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize

Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 15

编辑推荐

Metrics