全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Arabidopsis Heterotrimeric G-Proteins Play a Critical Role in Host and Nonhost Resistance against Pseudomonas syringae Pathogens

DOI: 10.1371/journal.pone.0082445

Full-Text   Cite this paper   Add to My Lib

Abstract:

Heterotrimeric G-proteins have been proposed to be involved in many aspects of plant disease resistance but their precise role in mediating nonhost disease resistance is not well understood. We evaluated the roles of specific subunits of heterotrimeric G-proteins using knock-out mutants of Arabidopsis Gα, Gβ and Gγ subunits in response to host and nonhost Pseudomonas pathogens. Plants lacking functional Gα, Gβ and Gγ1Gγ2 proteins displayed enhanced bacterial growth and disease susceptibility in response to host and nonhost pathogens. Mutations of single Gγ subunits Gγ1, Gγ2 and Gγ3 did not alter bacterial disease resistance. Some specificity of subunit usage was observed when comparing host pathogen versus nonhost pathogen. Overexpression of both Gα and Gβ led to reduced bacterial multiplication of nonhost pathogen P. syringae pv. tabaci whereas overexpression of Gβ, but not of Gα, resulted in reduced bacterial growth of host pathogen P. syringae pv. maculicola, compared to wild-type Col-0. Moreover, the regulation of stomatal aperture by bacterial pathogens was altered in Gα and Gβ mutants but not in any of the single or double Gγ mutants. Taken together, these data substantiate the critical role of heterotrimeric G-proteins in plant innate immunity and stomatal modulation in response to P. syringae.

References

[1]  Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56: 615-649. doi:10.1146/annurev.bi.56.070187.003151. PubMed: 3113327.
[2]  Temple BR, Jones AM (2007) The plant heterotrimeric G-protein complex. Annu Rev Plant Biol 58: 249-266. doi:10.1146/annurev.arplant.58.032806.103827. PubMed: 17201690.
[3]  Zhang H, Gao Z, Zheng X, Zhang Z (2012) The role of G-proteins in plant immunity. Plant Signal Behav 7: 1284-1288. doi:10.4161/psb.21431. PubMed: 22895102.
[4]  Neubig RR, Siderovski DP (2002) Regulators of G-protein signalling as new central nervous system drug targets. Nat Rev Drug Discov 1: 187-197. doi:10.1038/nrd747. PubMed: 12120503.
[5]  Oldham WM, Hamm HE (2008) Heterotrimeric G protein activation by G-protein-coupled receptors. Nat Rev Mol Cell Biol 9: 60-71. doi:10.1038/nrm2299. PubMed: 18043707.
[6]  Ma H, Yanofsky MF, Meyerowitz EM (1990) Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci U S A 87: 3821-3825. doi:10.1073/pnas.87.10.3821. PubMed: 2111018.
[7]  Weiss CA, Garnaat CW, Mukai K, Hu Y, Ma H (1994) Isolation of cDNAs encoding guanine nucleotide-binding protein beta-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc Natl Acad Sci U S A 91: 9554-9558. doi:10.1073/pnas.91.20.9554. PubMed: 7937804.
[8]  Trusov Y, Zhang W, Assmann SM, Botella JR (2008) Ggamma1 + Ggamma2 not equal to Gbeta: heterotrimeric G protein Ggamma-deficient mutants do not recapitulate all phenotypes of Gbeta-deficient mutants. Plant Physiol 147: 636-649. doi:10.1104/pp.108.117655. PubMed: 18441222.
[9]  Thung L, Trusov Y, Chakravorty D, Botella JR (2012) Ggamma1+Ggamma2+Ggamma3=Gbeta: the search for heterotrimeric G-protein gamma subunits in Arabidopsis is over. J Plant Physiol 169: 542-545. doi:10.1016/j.jplph.2011.11.010. PubMed: 22209167.
[10]  Llorente F, Alonso-Blanco C, Sánchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43: 165-180. doi:10.1111/j.1365-313X.2005.02440.x. PubMed: 15998304.
[11]  Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM et al. (2006) Heterotrimeric G proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol 140: 210-220. PubMed: 16339801.
[12]  Liu J, Ding P, Sun T, Nitta Y, Dong O et al. (2013) Heterotrimeric G proteins serve as a converging point in plant defense signaling activated by multiple receptor-like kinases. Plant Physiol, 161: 2146–58. PubMed: 23424249.
[13]  Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. doi:10.1038/nature05286. PubMed: 17108957.
[14]  Zeng W, He SY (2010) A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol 153: 1188-1198. doi:10.1104/pp.110.157016. PubMed: 20457804.
[15]  Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247-1256. doi:10.1038/cdd.2011.37. PubMed: 21475301.
[16]  Zurbriggen MD, Carrillo N, Tognetti VB, Melzer M, Peisker M et al. (2009) Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J 60: 962-973. doi:10.1111/j.1365-313X.2009.04010.x. PubMed: 19719480.
[17]  Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu Rev Phytopathol 51: 407-427. doi:10.1146/annurev-phyto-082712-102319. PubMed: 23725473.
[18]  Li X, Lin H, Zhang W, Zou Y, Zhang J et al. (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci U S A 102: 12990-12995. doi:10.1073/pnas.0502425102. PubMed: 16123135.
[19]  Truman W, de Zabala MT, Grant M (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46: 14-33. doi:10.1111/j.1365-313X.2006.02672.x. PubMed: 16553893.
[20]  Zhang J, Lu H, Li X, Li Y, Cui H et al. (2010) Effector-triggered and pathogen-associated molecular pattern-triggered immunity differentially contribute to basal resistance to Pseudomonas syringae. Mol Plant Microbe Interact 23: 940-948. doi:10.1094/MPMI-23-7-0940. PubMed: 20521956.
[21]  Rojas CM, Senthil-Kumar M, Wang K, Ryu CM, Kaundal A et al. (2012) Glycolate oxidase modulates reactive oxygen species-mediated signal transduction during nonhost resistance in Nicotiana benthamiana and Arabidopsis. Plant Cell 24: 336-352. doi:10.1105/tpc.111.093245. PubMed: 22286136.
[22]  Senthil-Kumar M, Mysore KS (2012) Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant Cell Environ 35: 1329-1343. doi:10.1111/j.1365-3040.2012.02492.x. PubMed: 22321246.
[23]  Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973-977. doi:10.1038/nature02076. PubMed: 14586469.
[24]  Kwon C, Neu C, Pajonk S, Yun HS, Lipka U et al. (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451: 835-840. doi:10.1038/nature06545. PubMed: 18273019.
[25]  Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M et al. (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183. doi:10.1126/science.1119409. PubMed: 16293760.
[26]  Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A et al. (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731-746. doi:10.1105/tpc.105.038372. PubMed: 16473969.
[27]  Underwood W, Somerville SC (2013) Perception of conserved pathogen elicitors at the plasma membrane leads to relocalization of the Arabidopsis PEN3 transporter. Proc Natl Acad Sci U S A 110: 12492-12497. doi:10.1073/pnas.1218701110. PubMed: 23836668.
[28]  Pinosa F, Buhot N, Kwaaitaal M, Fahlberg P, Thordal-Christensen H et al. (2013) Arabidopsis phospholipase ddelta is involved in Basal defense and nonhost resistance to powdery mildew fungi. Plant Physiol 163: 896-906. doi:10.1104/pp.113.223503. PubMed: 23979971.
[29]  Maeda K, Houjyou Y, Komatsu T, Hori H, Kodaira T et al. (2010) Nonhost resistance to Magnaporthe oryzae in Arabidopsis thaliana. Plant Signal Behav 5: 755-756. doi:10.4161/psb.5.6.11770. PubMed: 20404515.
[30]  Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H et al. (2002) The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci U S A 99: 13307-13312. doi:10.1073/pnas.192244099. PubMed: 12237405.
[31]  Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG et al. (2007) Heterotrimeric G protein gamma subunits provide functional selectivity in Gbetagamma dimer signaling in Arabidopsis. Plant Cell 19: 1235-1250. doi:10.1105/tpc.107.050096. PubMed: 17468261.
[32]  Zhang H, Wang M, Wang W, Li D, Huang Q et al. (2012) Silencing of G proteins uncovers diversified plant responses when challenged by three elicitors in Nicotiana benthamiana. Plant Cell Environ 35: 72-85. doi:10.1111/j.1365-3040.2011.02417.x. PubMed: 21895695.
[33]  Zhang W, He SY, Assmann SM (2008) The plant innate immunity response in stomatal guard cells invokes G-protein-dependent ion channel regulation. Plant J 56: 984-996. doi:10.1111/j.1365-313X.2008.03657.x. PubMed: 18702674.
[34]  Torres MA, Morales J, Sánchez-Rodríguez C, Molina A, Dangl JL (2013) Functional interplay between Arabidopsis NADPH oxidases and heterotrimeric G protein. Mol Plant Microbe Interact, 26: 686–94. PubMed: 23441575.
[35]  Lorek J, Griebel T, Jones AM, Kuhn H, Panstruga R (2013) The role of Arabidopsis heterotrimeric G-protein subunits in MLO2 function and MAMP-triggered immunity. Mol Plant Microbe Interact, 26: 991–1003. PubMed: 23656333.
[36]  Debener T, Lehnackers H, Arnold M, Dangl JL (1991) Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant J 1: 289-302. doi:10.1046/j.1365-313X.1991.t01-7-00999.x. PubMed: 21736648.
[37]  Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46: 101-122. doi:10.1146/annurev.phyto.121107.104959. PubMed: 18422426.
[38]  Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312: 264-266. doi:10.1126/science.1123769. PubMed: 16614222.
[39]  Fan LM, Zhang W, Chen JG, Taylor JP, Jones AM et al. (2008) Abscisic acid regulation of guard-cell K+ and anion channels in Gbeta- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci U S A 105: 8476-8481. doi:10.1073/pnas.0800980105. PubMed: 18541915.
[40]  Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB et al. (2011) An atypical heterotrimeric G-protein gamma-subunit is involved in guard cell K(+)-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67: 840-851. doi:10.1111/j.1365-313X.2011.04638.x. PubMed: 21575088.
[41]  Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980. doi:10.1016/j.cell.2006.06.054. PubMed: 16959575.
[42]  Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205-227. doi:10.1146/annurev.phyto.43.040204.135923. PubMed: 16078883.
[43]  Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013) Tell me more: roles of NPRs in plant immunity. Trends Plant Sci, 18: 402–11. PubMed: 23683896.
[44]  Yang DL, Yang Y, He Z (2013) Roles of plant hormones and their interplay in rice immunity. Mol Plant 6: 675-685. doi:10.1093/mp/sst056. PubMed: 23589608.
[45]  Okamoto H, G?bel C, Capper RG, Saunders N, Feussner I et al. (2009) The alpha-subunit of the heterotrimeric G-protein affects jasmonate responses in Arabidopsis thaliana. J Exp Bot 60: 1991-2003. doi:10.1093/jxb/erp060. PubMed: 19342430.
[46]  Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011. doi:10.1016/S1097-2765(00)80265-8. PubMed: 10911994.
[47]  Li W, Ahn IP, Ning Y, Park CH, Zeng L et al. (2012) The U-Box/ARM E3 ligase PUB13 regulates cell death, defense, and flowering time in Arabidopsis. Plant Physiol 159: 239-250. doi:10.1104/pp.111.192617. PubMed: 22383540.
[48]  Li J, Wen J, Lease KA, Doke JT, Tax FE et al. (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110: 213-222. doi:10.1016/S0092-8674(02)00812-7. PubMed: 12150929.
[49]  Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110: 203-212. doi:10.1016/S0092-8674(02)00814-0. PubMed: 12150928.
[50]  Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA et al. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22: 2623-2633. doi:10.1093/emboj/cdg277. PubMed: 12773379.
[51]  Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14: 3089-3099. doi:10.1105/tpc.007906. PubMed: 12468729.
[52]  Chen JG, Gao Y, Jones AM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141: 887-897. doi:10.1104/pp.106.079202. PubMed: 16679415.
[53]  Assmann SM (2002) Heterotrimeric and unconventional GTP binding proteins in plant cell signaling. Plant Cell 14 Suppl: S355-S373. PubMed: 12045288.
[54]  Hurowitz EH, Melnyk JM, Chen YJ, Kouros-Mehr H, Simon MI et al. (2000) Genomic characterization of the human heterotrimeric G protein alpha, beta, and gamma subunit genes. DNA Res 7: 111-120. doi:10.1093/dnares/7.2.111. PubMed: 10819326.
[55]  Pandey S, Chen JG, Jones AM, Assmann SM (2006) G-protein complex mutants are hypersensitive to abscisic acid regulation of germination and postgermination development. Plant Physiol 141: 243-256. doi:10.1104/pp.106.079038. PubMed: 16581874.
[56]  Pandey S, Wang RS, Wilson L, Li S, Zhao Z et al. (2010) Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Mol Syst Biol 6: 372. PubMed: 20531402.
[57]  Spiegel AM (1996) Defects in G protein-coupled signal transduction in human disease. Annu Rev Physiol 58: 143-170. doi:10.1146/annurev.ph.58.030196.001043. PubMed: 8815789.
[58]  Farfel Z, Bourne HR, Iiri T (1999) The expanding spectrum of G protein diseases. N Engl J Med 340: 1012-1020. doi:10.1056/NEJM199904013401306. PubMed: 10099144.
[59]  Ropers HH, Hamel BC (2005) X-linked mental retardation. Nat Rev Genet 6: 46-57. doi:10.1038/nrg1501. PubMed: 15630421.
[60]  Melien O (2007) Heterotrimeric G proteins and disease. Methods Mol Biol 361: 119-144. PubMed: 17172709.
[61]  Sharp GW, Hynie S (1971) Stimulation of intestinal adenyl cyclase by cholera toxin. Nature 229: 266-269. doi:10.1038/229266a0. PubMed: 4323551.
[62]  Legendre L, Heinstein PF, Low PS (1992) Evidence for participation of GTP-binding proteins in elicitation of the rapid oxidative burst in cultured soybean cells. J Biol Chem 267: 20140-20147. PubMed: 1400332.
[63]  Lieberherr D, Thao NP, Nakashima A, Umemura K, Kawasaki T, et al. (2005) A sphingolipid elicitor-inducible mitogen-activated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G-protein in rice 1 [w]. Plant Physiol 138: 1644-1652.
[64]  Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K et al. (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci U S A 103: 230-235. doi:10.1073/pnas.0509875103. PubMed: 16380417.
[65]  Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135: 1447-1456. doi:10.1104/pp.103.036384. PubMed: 15220467.
[66]  Ishiga Y, Ishiga T, Uppalapati SR, Mysore KS (2011) Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions. Plant Methods 7: 32. doi:10.1186/1746-4811-7-32. PubMed: 21978451.
[67]  Nilson SE, Assmann SM (2010) The alpha-subunit of the Arabidopsis heterotrimeric G protein, GPA1, is a regulator of transpiration efficiency. Plant Physiol 152: 2067-2077. doi:10.1104/pp.109.148262. PubMed: 20200073.
[68]  Trusov Y, Chakravorty D, Botella JR (2012) Diversity of heterotrimeric G-protein gamma subunits in plants. BMC Res Notes 5: 608. doi:10.1186/1756-0500-5-608. PubMed: 23113884.
[69]  Clapham DE, Neer EJ (1997) G protein beta gamma subunits. Annu Rev Pharmacol Toxicol 37: 167-203. doi:10.1146/annurev.pharmtox.37.1.167. PubMed: 9131251.
[70]  Chakravorty D, Trusov Y, Zhang W, Acharya BR, Sheahan MB et al. (2011) An atypical heterotrimeric G-protein ?-subunit is involved in guard cell K+-channel regulation and morphological development in Arabidopsis thaliana. Plant J 67: 840-851. doi:10.1111/j.1365-313X.2011.04638.x. PubMed: 21575088.
[71]  Roy Choudhury S, Riesselman AJ, Pandey S (2013) Constitutive or seed-specific overexpression of Arabidopsis G-protein ?-subunit 3 (AGG3) results in increased seed and oil production and improved stress tolerance in Camelina sativa. Plant Biotechnology Journal.
[72]  Lee S, Choi H, Suh S, Doo IS, Oh KY et al. (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121: 147-152. doi:10.1104/pp.121.1.147. PubMed: 10482669.
[73]  Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ et al. (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol 7: e1000139. PubMed: 19564897.
[74]  Lee S, Ishiga Y, Clermont K, Mysore KS (2013) Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens. PeerJ 1: e34. doi:10.7717/peerj.34. PubMed: 23638370.
[75]  Lee S, Yang DS, Uppalapati SR, Sumner LW, Mysore KS (2013) Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol 13: 65. doi:10.1186/1471-2229-13-65. PubMed: 23597256.
[76]  Desclos-Theveniau M, Arnaud D, Huang TY, Lin GJ, Chen WY et al. (2012) The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog 8: e1002513. PubMed: 22346749.
[77]  Gao Y, Wang S, Asami T, Chen JG (2008) Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein alpha subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. Plant Cell Physiol 49: 1013-1024. doi:10.1093/pcp/pcn078. PubMed: 18499742.
[78]  Oki K, Inaba N, Kitagawa K, Fujioka S, Kitano H et al. (2009) Function of the alpha subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol 50: 161-172. doi:10.1093/pcp/pcn182. PubMed: 19036785.
[79]  Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S et al. (2012) Brassinosteroids inhibit pathogen-associated molecular pattern–triggered immune signaling independent of the receptor kinase BAK1. Proceedings of the National Academy of Sciences of the USA 109: 303-308. doi:10.1073/pnas.1109921108.
[80]  Belkhadir Y, Wang X, Chory J (2006) Brassinosteroid Signaling Pathway. Sci STKE 2006: cm4-.
[81]  Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476. doi:10.1105/tpc.105.036574. PubMed: 16377758.
[82]  Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105: 7100-7105. doi:10.1073/pnas.0802332105. PubMed: 18458331.
[83]  He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128: 876-884. doi:10.1104/pp.010843. PubMed: 11891244.
[84]  Creelman RA, Mullet JE (1997) BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol 48: 355-381. doi:10.1146/annurev.arplant.48.1.355. PubMed: 15012267.
[85]  Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV (2005) Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17: 957-970. doi:10.1105/tpc.104.029603. PubMed: 15705948.
[86]  Zeng W, Melotto M, He SY (2010) Plant stomata: a checkpoint of host immunity and pathogen virulence. Curr Opin Biotechnol 21: 599-603. doi:10.1016/j.copbio.2010.05.006. PubMed: 20573499.
[87]  Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284. doi:10.1046/j.1365-313X.1999.00451.x. PubMed: 10377993.
[88]  Ishiga Y, Ishiga T, Uppalapati SR, Mysore KS (2011) Arabidopsis seedling-flood inoculation technique: A rapid and reliable assay for studying plant-host/nonhost bacterial pathogen interactions. . Plant. Methods.
[89]  Gudesblat GE, Torres PS, Vojnov AA (2009) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149: 1017-1027. PubMed: 19091877.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133