期刊论文详细信息
BMC Genomics
Analysis of root proteome unravels differential molecular responses during compatible and incompatible interaction between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceri Race1 (Foc1)
Sampa Das1  Debabrata Basu1  Dipankar Chakraborti2  Anirban Bhar1  Sumanti Gupta1  Moniya Chatterjee1 
[1] Authors Address: Division of Plant Biology, Bose Institute, Centenary Campus, P 1/12, CIT Scheme, VII-M, Kankurgachi, Kolkata 700054, West Bengal, India;Post Graduate Department of Biotechnology, St. Xavier’s College (Autonomous), 30 Park Street, Kolkata 700016, India
关键词: Root proteomics;    Defense response;    Fusarium oxysporum f. sp. ciceri Race 1(Foc1);    Chickpea (Cicer arietinum L.);   
Others  :  1127800
DOI  :  10.1186/1471-2164-15-949
 received in 2014-05-26, accepted in 2014-10-22,  发布年份 2014
PDF
【 摘 要 】

Background

Vascular wilt caused by Fusarium oxysporum f. sp. ciceri Race 1 (Foc1) is a serious disease of chickpea (Cicer arietinum L.) accounting for approximately 10-15% annual crop loss. The fungus invades the plant via roots, colonizes the xylem vessels and prevents the upward translocation of water and nutrients, finally resulting in wilting of the entire plant. Although comparative transcriptomic profiling have highlighted some important signaling molecules, but proteomic studies involving chickpea-Foc1 are limited. The present study focuses on comparative root proteomics of susceptible (JG62) and resistant (WR315) chickpea genotypes infected with Foc1, to understand the mechanistic basis of susceptibility and/or resistance.

Results

The differential and unique proteins of both genotypes were identified at 48 h, 72 h, and 96 h post Foc1 inoculation. 2D PAGE analyses followed by MALDI-TOF MS and MS/MS identified 100 differentially (>1.5 fold<, p < 0.05) or uniquely expressed proteins. These proteins were further categorized into 10 functional classes and grouped into GO (gene ontology) categories. Network analyses of identified proteins revealed intra and inter relationship of these proteins with their neighbors as well as their association with different defense signaling pathways. qRT-PCR analyses were performed to correlate the mRNA and protein levels of some proteins of representative classes.

Conclusions

The differential and unique proteins identified indicate their involvement in early defense signaling of the host. Comparative analyses of expression profiles of obtained proteins suggest that albeit some common components participate in early defense signaling in both susceptible and resistant genotypes, but their roles and regulation differ in case of compatible and/or incompatible interactions. Thus, functional characterization of identified PR proteins (PR1, BGL2, TLP), Trypsin protease inhibitor, ABA responsive protein, cysteine protease, protein disulphide isomerase, ripening related protein and albumins are expected to serve as important molecular components for biotechnological application and development of sustainable resistance against Foc1.

【 授权许可】

   
2014 Chatterjee et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150221102739732.pdf 3584KB PDF download
Figure 5. 68KB Image download
Figure 4. 135KB Image download
Figure 3. 235KB Image download
Figure 2. 55KB Image download
Figure 1. 62KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Richard J, Panstruga R: Tête à tête inside a plant cell:establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 2006, 171:699-718.
  • [2]Tsuda K, Katagiri F: Comparing signaling mechanisms engaged in pattern triggered & effector triggered immunity. Curr Opin Plant Biol 2010, 13:459-465.
  • [3]Buchanan BB, Gruissem W, Jones RL: Biochemistry and Molecular Biology of Plants. New Delhi: IK International; 2007.
  • [4]Jones JDG, Dangl JL: The plant immune system. Nature 2006, 444:323-329.
  • [5]Thomma BPHJ, Nu¨rnberger T, Joosten MHAJ: Of PAMPs and effectors: The blurred PTI-ETI dichotomy. Plant Cell 2011, 23:4-15.
  • [6]Lavin M, Herendeen PS, Wojciechowski MF: Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 2005, 54:575-594.
  • [7]Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Reid DE, Gresshoff PM: Molecular analysis of legume nodule development and autoregulation. J. Integrative Plant Biol 2010, 52:61-76.
  • [8]Haware MP, Nene YL: Races of Fusarium oxysporum. Plant Dis 1982, 66:809-810.
  • [9]Jime’nez-Gasco MM, Navas-Cortes JA, Jime’nez-Diaz RM: The Fusarium oxysporum f. sp. ciceris/Cicer arietinum pathosystem: a case study of the evolution of plant-pathogenic fungi into races and pathotypes. Internat Microbiol 2004, 7:95-104.
  • [10]Gupta S, Bhar A, Das S: Understanding the molecular defence responses of host during chickpea–Fusarium interplay: where do we stand? Funct Plant Biol 2013. doi.org/10.1071/FP13063
  • [11]Nimalkar SB, Harsulkar AM, Giri AP, Sainani MN, Franceshi V, Gupta VS: Differentially expressed gene transcripts in roots of resistant and susceptible chickpea plant (Cicer arietinum L.) upon Fusarium oxysporum infection. Physiol Mol Plant Pathol 2006, 68:176-188.
  • [12]Hossain MM, Hossain N, Sultana F, Islam SMN, Islam MS, Bhuiyan MKA: Integrated management of Fusarium wilt of chickpea (Cicer arietinum L.) caused by Fusarium oxysporum f. sp. ciceris with microbial antagonist, botanical extract and fungicide. Afr J Biotechnol 2013, 12:4699-4706.
  • [13]Berrocal-Lobo M, Molina A: Arabidopsis defense response against Fusarium oxysporum. Cell 2007, 13:145-150.
  • [14]Van der Does HC, Duyvesteijn RG, Goltstein PM, van Schie CC, Manders EM, Cornelissen BJ, Rep M: Expression of effector gene SIX1 of Fusarium oxysporum requires living plant cells. Fungal Genet Biol 2008, 45:1257-1264.
  • [15]Gupta S, Chakraborti D, Rangi RK, Basu D, Das S: A molecular insight into the early events of chickpea (Cicer arietinum) and Fusarium oxysporum f. sp. ciceri (race 1) interaction through cDNA AFLP analysis. Phytopathology 2009, 99:1245-1257.
  • [16]Gupta S, Chakraborti D, Sengupta A, Basu D, Das S: Primary metabolism of chickpea is the initial target of wound inducing early sensed Fusarium oxysporum f. sp. ciceri race 1. PLoS One 2010, 5:e9030. doi:10.1371/journal.pone.0009030
  • [17]Gupta S, Bhar A, Chatterjee M, Das S: Fusarium oxysporum f.sp. ciceri Race 1 induced redox state alterations are coupled to downstream defense signaling in root tissues of chickpea (Cicer arietinum L.). PLoS One 2013, 8:e73163. doi:10.1371/journal.pone.0073163
  • [18]Ashraf N, Ghai D, Barman P, Basu S, Gangisetty N, Mandal MK, Chakraborty N, Datta A, Chakraborty S: Comparative analyses of genotype dependent expressed sequence tags and stress-responsive transcriptome of chickpea wilt illustrate predicted and unexpected genes and novel regulators of plant immunity. BMC Genomics 2009, 10:e415. BioMed Central Full Text
  • [19]Giri AP, Harsulkar AM, Patankar AG, Gupta VS, Sainani MN, Deshpande VV, Ranjeka PK: Association of induction of protease and chitinase in chickpea roots with resistance to Fusarium oxysporum. f.sp. ciceris. Plant Pathol 1998, 47:693-699.
  • [20]Cho S, Muehlbauer FJ: Genetic effect of differentially regulated fungal response genes on resistance to necrotrophic fungal pathogens in chickpea (Cicer arietinum L.). Physiol Mol Plant Pathol 2004, 64:57-66.
  • [21]Flandez-Galvez H, Ford R, Pang ECK, Taylor PWJ: An intraspecific linkage map of chickpea (Cicer arietinum L.) genome based on sequence tagged microsatellite site and resistant gene analogue markers. Theo Appl Genet 2003, 106:1447-1456.
  • [22]Jorrín JV, Rubiales D, Dumas-Gaudot E, Recorbet G, Maldonado A, Castillejo MA, Curto M: Proteomics: a promising approach to study biotic interaction in legumes.A review. Euphytica 2006, 147:37-47.
  • [23]Padliya ND, Cooper B: Mass spectrometry-based proteomics for the detection of plant pathogens. Proteomics 2006, 6:4069-4075.
  • [24]Asano T, Makota K, Takumi N: The defense response in Arabidopsis thaliana against Fusarium sporotrichoides. Proc Natl Acad Sci U S A 2012, 10:61.
  • [25]Castillejo MA, Maldonado AM, Dumas-Gaudot E, Fernandez-Aparico M, Susin R, Diego R, Jorrin JV: Differential expression proteomics to investigate responses and resistance to Orobanche crenata in Medicago trancatula. BMC Genomics 2009, 10:294. BioMed Central Full Text
  • [26]Carpentier SC, Panis B, Vertommen A, Swennen R, Sergeant K, Renaut J, Laukens K, Witters E, Samyn B, Devreese B: Proteome analysis of non-model plants: a challenging but powerful approach. Mass Spectrom Rev 2008, 27:354-377.
  • [27]Summerell BA, Sallen B, Leslie JF: A utilitarian approach to Fusarium identification. Plant Dis 2003, 87:117-128.
  • [28]Subba P, Barua P, Kumar R, Datta A, Soni KK, Chakraborty S, Chakraborty N: Phosphoproteomic dynamics of chickpea (Cicer arietinum L.) reveals shared and distinct components of dehydration response. J Proteome Res 2013, 12:5025-5047.
  • [29]Chatterjee M, Gupta S, Bhar A, Das S: Optimization of an efficient protein extraction protocol compatible with two-dimensional electrophoresis and mass spectrometry from recalcitrant phenolic rich roots of chickpea (Cicer arietinum L.). Int J Proteomics 2012, 2012:536963. doi:10.1155/2012/536963
  • [30]Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
  • [31]Valledor L, Jorrín J: Back to the basics: Maximizing the information obtained by quantitative two dimensional gel electrophoresis analyses by an appropriate experimental design and statistical analyses. J Proteomics 2011, 74:1-18.
  • [32]Shevchenko A, Tomas H, Havliˇs J, Olsen JV, Mann M: In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2007, 1:2856-2860.
  • [33]Nikitin A, Egorov S, Daraselia N, Mazo I: Pathway studio–the analysis and navigation of molecular networks. Bioinformatics 2003, 19:2155-2157.
  • [34]Garg R, Sahoo A, Tyagi AK, Jain M: Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Comm 2010, 396:283-288.
  • [35]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods 2001, 25:402-408.
  • [36]Chattopadhyay A, Subba P, Pandey A, Bhushan D, Kumar R, Datta A, Chakraborty S, Chakraborty N: Analysis of the grasspea proteome and identification of stress-responsive proteins upon exposure to high salinity, low temperature, and abscisic acid treatment. Phytochemistry 2011, 72:1293-1307.
  • [37]Subba P, Kumar R, Gayali S, Shekhar S, Parveen S, Pandey A, Datta A, Chakraborty S, Chakraborty N: Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar. Proteomics 2013, 13:1973-1992.
  • [38]Schlüter H, Apweiler R, Holzhütter HG, Jungblut PR: Finding one’s way in proteomics: a protein species nomenclature. Chem Cent J 2009, 3:11. BioMed Central Full Text
  • [39]Zelko IN, Mariani TJ, Folz RJ: Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 2002, 33:337-349.
  • [40]Pandey A, Choudhary MK, Bhushan D, Chattopadhyay A, Chakraborty S, Datta A, Chakraborty N: The nuclear proteome of chickpea (Cicer arietinum L.) reveals predicted and unexpected proteins. J Proteome Res 2006, 5:3301-3311.
  • [41]Aboul-Soud MAM, Chen X, Kang JG, Yun BW, Raja MU, Malik SI, Loake GJ: Activation tagging of ADR2 conveys a spreading lesion phenotype and resistance to biotrophic pathogens. New Phytol 2009, 183:1163-1175.
  • [42]Lu H, Rate DN, Song JT, Greenberg JT: ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 2003, 15:2408-2420.
  • [43]Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, MacKinlay J, Loake GJ, Mundy J, Morris PC: Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 2008, 148:212-222.
  • [44]Ferrari S, Plotnikova JM, Lorenzo GD, Ausubel FM: Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 2003, 35:193-205.
  • [45]Vorwerk S, Schiff C, Santamaria M, Koh S, Nishimura M, Vogel J, Somerville C, Somerville S: EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol 2007, 7:35. doi:10.1186/1471-2229-7-35 BioMed Central Full Text
  • [46]Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X: Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 2006, 48:647-656.
  • [47]Laxalt AM, Raho N, Have AT, Lamattina L: Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J Biol Chem 2007, 282:21160-21168.
  • [48]Nandi A, Krothapalli K, Buseman CM, Li M, Welti R, Enyedi A, Shah J: Arabidopsis sfd mutants affect plastidic lipid composition and suppress dwarfing, cell death, and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell 2003, 15:2383-2398.
  • [49]Sandhu D, Tasma IM, Frasch R, Bhattacharyya MK: Systemic acquired resistance in soybean is regulated by two proteins, orthologous to Arabidopsis NPR1. BMC Plant Biol 2009, 9:105. doi:10.1186/1471-2229-9-105 BioMed Central Full Text
  • [50]Lee JH, Kim WT: Molecular and biochemical characterization of VR-EILs encoding mung bean ETHYLENE INSENSITIVE3-LIKE proteins. Plant Physiol 2003, 132:1475-1488.
  • [51]Demkura PV, Abdala G, Baldwin IT, Ballare CL: Jasmonate-dependent and independent pathways mediate specific effects of solar ultraviolet-B radiation on leaf phenolics and antiherbivore defense. Plant Physiol 2010, 152:1084-1095.
  • [52]Skibbe M, Qu N, Galis I, Baldwin IT: Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 2008, 20:1984-2000.
  • [53]Coram TE, Settles ML, Chen X: Transcriptome analysis of high temperature adult plant resistance conditioned by Yr39 during wheat-Pucinia striiformis f.sp. tritici interaction. Molecular Plant Pathol 2008, 9:479-493.
  • [54]Matyalman D, Mert Z, Baykal AT, Inan C, Gunel A, Hasancebi S: Proteomic analysis of early responsive resistance proteins of wheat (Triticum aestivum) to yellow rust (Puccinia striiformis F.Sp. tritici) using ProteomeLab PF2D. Plant Omics J 2013, 6:24-35.
  • [55]Alscher RG, Erturk N, Heath LS: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 2002, 53:1331-1341.
  • [56]Takemoto D, Hardham AR, Jones DA: Differences in cell death induction by phytophthora elicitins are determined by signal components downstream of MAP Kinase Kinase in different species of Nicotiana and Cultivars of Brassica rapa and Raphanus sativus. Plant Physiol 2005, 138:1491-1504.
  • [57]Narendra S, Venkataramani S, Shen G, Wang J, Pasapula V, Lin Y, Kornyeyev D, Holaday AS, Zhang H: The Arabidopsis ascorbate peroxidase 3 is a peroxisomal membrane-bound antioxidant enzyme and is dispensable for Arabidopsis growth and development. J Exp Bot 2006, 57:3033-3042.
  • [58]Panchuk II, Volkov RA, Schoffl F: Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 2002, 129:838-853.
  • [59]Dean JD, Goodwin PH, Hsiang T: Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot 2005, 56:1525-1533.
  • [60]Vieira Dos Santos C, Rey P: Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci 2006, 11:329-334.
  • [61]Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H: Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 2005, 44:653-668.
  • [62]Hodges DM, Forney CF: The effects of ethylene, depressed oxygen and elevated carbon dioxide on antioxidant profiles of senescing spinach leaves. J Exp Bot 2000, 51:645-655.
  • [63]Zhu H, Li GJ, Ding L, Cui X, Berg H, Assmann SM, Xia Y: Arabidopsis extra large G-protein 2 (XLG2) interacts with the G beta subunit of heterotrimeric G protein and functions in disease resistance. Mol Plant 2009, 2:513-525.
  • [64]Fan LM, Zhang W, Chen JG, Taylor JP, Jones AM, Assmann SM: Abscisic acid regulation of guard-cell K+ and anion channels in G beta- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci 2008, 105:8476-8481.
  • [65]Gorecka KM, Thouverey C, Buchet R, Pikula S: Potential role of annexin AnnAt1 from Arabidopsis thaliana in pH-mediated cellular response to environmental stimuli. Plant Cell Physiol 2007, 48:792-803.
  • [66]Laohavisit A, Mortimer JC, Demidchik V, Coxon KM, Stancombe MA, Macpherson N, Brownlee C, Hofmann A, Webb AAR, Miedema H, Battey NH, Davies JM: Zea mays annexins modulate cytosolic free Ca and generate a Ca2+ -permeable conductance. Plant Cell 2009, 21:479-493.
  • [67]Ghelis T, Dellis O, Jeannette E, Bardat F, Miginiac E, Sotta B: Abscisic acid plasmalemma perception triggers a calcium influx essential for RAB18 gene expression in Arabidopsis thaliana suspension cells. FEBS Lett 2000, 483:67-70.
  • [68]Hallouin M, Ghelis T, Brault M, Bardat F, Cornel D, Miginiac E, Rona JP, Sotta B, Jeannette E: Plasmalemma abscisic acid perception leads to RAB18 expression via phospholipase D activation in Arabidopsis suspension cells. Plant Physiol 2002, 130:265-272.
  • [69]Lee Y, Lee HS, Lee JS, Kim SK, Kim SH: Hormone and light-regulated nucleocytoplasmic transport in plants: current status. J Exp Bot 2008, 59:3229-3245.
  • [70]Dhar-Chowdhury P, Harrell MD, Han SY, Jankowska D, Parachuru L, Morrissey A, Srivastava S, Liu W, Malester B, Yoshida H, Coetzee WA: The glycolytic enzymes, glyceraldehyde-3-phosphate dehydrogenase, triose-phosphate isomerase, and pyruvate kinase are components of the K (ATP) channel macromolecular complex and regulate its function. J Biol Chem 2005, 280:38464-38470.
  • [71]Tovar-Mendez A, Miernyk JA, Randall DD: Regulation of pyruvate dehydrogenase complex activity in plant cells. Eur J Biochem 2003, 270:1043-1049.
  • [72]Ga’lvez L, Gonza’lez EM, Arrese-Igor C: Evidence for carbon flux shortage and strong carbon/nitrogen interactions in pea nodules at early stages of water stress. J Exp Bot 2005, 56:2551-2561.
  • [73]Nunes-Nesi A, Fernie AR, Stitt M: Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 2010, 3:973-996.
  • [74]Padmanaban S, Lin X, Perera I, Kawamura Y, Sze H: Differential expression of vacuolar H+ -ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiol 2004, 134:1514-1526.
  • [75]Lee A, Kirichenko A, Vygodina T, Siletsky SA, Das TK, Rousseau DL, Gennis R, Konstantinov AA: Ca(2+)-binding site in Rhodobacter sphaeroides cytochrome C oxidase. Biochemistry 2002, 41:8886-8898.
  • [76]Shindo T, Misas-Villamil JC, Horger AC, Song J, van der Hoorn RA: A role in immunity for Arabidopsis cysteine protease RD21, the ortholog of the tomato immune protease C14. PLoS One 2012, 7:e29317. doi:10.1371/journal.pone.0029317
  • [77]Ho C-L, Noji M, Saito M, Yamazaki M, Saito K: Molecular characterization of plastidic phosphoserine aminotransferase in serine biosynthesis from Arabidopsis. Plant J 1998, 16:443-452.
  • [78]Shen B, Li C, Tarczynski MC: High free-methionine and decreased lignin content result from a mutation in the Arabidopsis S-adenosyl-Lmethionine synthetase 3 gene. Plant J 2002, 29:371-380.
  • [79]Aoki T, Akashi T, Ayabe SI: Flavonoids of leguminous plants: structure, biological activity, and biosynthesis. J Plant Res 2000, 113:475-488.
  • [80]Pelloux J, Ruste’ rucci C, Mellerowicz EJ: New insights into pectin methylesterase structure and function. Trends Plant Sci 2007, 12:267-277.
  • [81]Yao C, Wu Y, Nie H, Tang D: RPN1a, a 26S proteasome subunit, is required for innate immunity in Arabidopsis. Plant J 2012, 71:1015-1028.
  • [82]Suty L, Lequeu J, Lançon A, Etienne P, Petitot AS, Blein JP: Preferential induction of 20S proteasome subunits during elicitation of plant defense reactions: towards the characterization of “plant defense proteasomes”. Int J Biochem Cell Biol 2003, 35:637-650.
  • [83]Moffatt BA, Wang L2, Allen MS, Stevens YY, Qin W, Snider J, von Schwartzenberg K: Adenosine kinase of Arabidopsis. Kinetic properties and gene expression. Plant Physiol 2000, 124:1775-1785.
  • [84]Lange PR, Geserick C, Tischendorf G, Zrenner R: Functions of chloroplastic adenylate kinases in Arabidopsis. Plant Physiol 2008, 146:492-504.
  • [85]Hopkins MT, Lampi Y, Wang TW, Liu Z, Thompson JE: Eukaryotic translation initiation factor 5A is involved in pathogen-induced cell death and development of disease symptoms in Arabidopsis. Plant Physiol 2008, 148:479-489.
  • [86]Ondzighi CA, Christopher DA, Cho EJ, Chang SC, Staehelin LA: Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 2008, 20:2205-2220.
  • [87]Rigobello MP, Donella-Deana A, Cesaro L, Bindoli A: Distribution of protein disulphide isomerase in rat liver mitochondria. Biochem J 2001, 356:567-570.
  • [88]Lytle BL, Song J, de la Cruz NB, Peterson FC, Johnson KA, Bingman CA, Phillips GN Jr, Volkman BF: Structures of two Arabidopsis thaliana major latex proteins represent novel helix-grip folds. Proteins 2009, 76:237-243.
  • [89]Carter C, Thornburg RW: Tobacco nectarin I. Purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues. J Biol Chem 2000, 275:36726-36733.
  • [90]Day B, Henty JL, Porter KJ, Staiger CJ: The pathogen-actin connection: a platform for defense signaling in plants. Annu Rev Phytopathol 2011, 49:483-506.
  • [91]Aroca R, Amodeo G, Ferna’ndez-Illescas S, Herman EM, Chaumont F, Chrispeels MJ: The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 2005, 137:341-353.
  • [92]Cândido Ede S, Pinto MF, Pelegrini PB, Lima TB, Silva ON, Pogue R, Grossi-de-Sá MF, Franco OL: Plant storage proteins with antimicrobial activity: novel insights into plant defense mechanisms. FASEB J 2011, 25:3290-3305.
  • [93]Varshney RK, Song C, Saxena RK, Azam S, Yu S, Sharpe AG, Cannon S, Baek J, Rosen BD, Tar’an B, Millan T, Zhang X, Ramsay LD, Iwata A, Wang Y, Nelson W, Farmer AD, Gaur PM, Soderlund C, Penmetsa RV, Xu C, Bharti AK, He W, Winter P, Zhao S, Hane JK, Carrasquilla-Garcia N, Condie JA, Upadhyaya HD, Luo MC, et al.: Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 2013, 3:240-246.
  • [94]Thompson CE, Fernandes CL, de Souza ON, Salzano FM, Bonatto SL, Freitas LB: Molecular modeling of pathogenesis-related proteins of family 5. Cell Biochem Biophys 2006, 44:385-394.
  • [95]Shibuya N, Minami E: Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant P 2001, 59:223-233.
  • [96]Dopico B1, Lowe AL, Wilson ID, Merodio C, Grierson D: Cloning and characterization of avocado fruit mRNAs and their expression during ripening and low-temperature storage. Plant Mol Biol 1993, 21:437-449.
  • [97]Hadfield KA1, Dang T, Guis M, Pech JC, Bouzayen M, Bennett AB: Characterization of ripening-regulated cDNAs and their expression in ethylene-suppressed charentais melon fruit. Plant Physiol 2000, 122:977-983.
  • [98]Choi DS, Hwang BK: Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 2011, 23:823-842.
  • [99]Fang X, Chen W, Xin Y, Zhang H, Yan C, Yu H, Liu H, Xiao W, Wang S, Zheng G, Liu H, Jin L, Ma H, Ruan S: Proteomic analysis of strawberry leaves infected with Colletotrichum fragariae. J Proteomics 2012, 75:4074-4090.
  • [100]Palomares-Rius JE, Castillo P, Navas-Cortés JA, Jiménez-Díaz RM, Tena M: A proteomic study of in-root interactions between chickpea pathogens: The root-knot nematode Meloidogyne artiellia and the soil-borne fungus Fusarium oxysporum f. sp. ciceris race 5. J Proteomics 2011, 74:2034-2051.
  文献评价指标  
  下载次数:36次 浏览次数:3次