1932

Abstract

Christopher John Lamb (1950–2009) made major contributions to the field of plant defense gene activation, particularly through his studies on signal transduction mechanisms. Between 1994 and 2004, he published a series of seminal papers that outlined the involvement of hydrogen peroxide, nitric oxide, lipid transfer proteins, and aspartic proteases as critical components of local and/or systemic resistance during plant-microbe interactions. Prior to this, he had been one of the first to establish the fact that induced defense responses resulted from transcriptional activation of sets of coordinately regulated genes. Chris obtained his B.S and PhD degrees in biochemistry from the University of Cambridge, United Kingdom, moving to the Botany School at the University of Oxford as a postdoctoral fellow in 1975 and to the Biochemistry Department in Oxford as a Departmental Demonstrator in 1978. He was appointed founding director of the Plant Biology Laboratory at the Salk Institute for Biological Studies in La Jolla, California in 1982, and occupied the last ten years of his life as Director of the John Innes Center, Norwich, United Kingdom. In spite of spending most of his career as a director at two of the world's most prestigious institutes, formal recognition of his achievements came late in life, with election to the Royal Society of London in 2008 and endowment of the honor of Commander of the British Empire (CBE) for his contributions to British plant science by Queen Elizabeth II in 2009. Sadly, Chris did not live to attend the official ceremony at which he would receive his CBE.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-072910-095224
2011-09-08
2024-10-07
Loading full text...

Full text loading...

/deliver/fulltext/phyto/49/1/annurev-phyto-072910-095224.html?itemId=/content/journals/10.1146/annurev-phyto-072910-095224&mimeType=html&fmt=ahah

Literature Cited

  1. Alvarez ME, Pennell R, Meijer P-J, Ishikawa A, Dixon RA, Lamb C. 1.  1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–84The seminal finding that inoculation at a single site can lead to systemic oxidative bursts that underlie the expression and spread of SAR. [Google Scholar]
  2. Arias JA, Dixon RA, Lamb CJ. 2.  1993. Dissection of the functional architecture of a plant defense gene promoter using a homologous in vitro transcription system. Plant Cell 5:485–96 [Google Scholar]
  3. Bate NJ, Orr J, Ni W, Meroni A, Nadler-Hassar T. 3.  et al. 1994. Quantitative relationship between phenylalanine ammonia-lyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate determining step in natural product synthesis. Proc. Natl. Acad. Sci. USA 91:7608–12 [Google Scholar]
  4. Baulcombe DC.4.  1996. RNA as a target and an initiator of post-transcriptional gene silencing in transgenic plants. Plant Mol. Biol. 32:79–88 [Google Scholar]
  5. Bell JN, Dixon RA, Bailey JA, Rowell PM, Lamb CJ. 5.  1984. Differential induction of chalcone synthase mRNA activity at the onset of phytoalexin accumulation in compatible and incompatible plant-pathogen interactions. Proc. Natl. Acad. Sci. USA 81:3384–88 [Google Scholar]
  6. Bell JN, Ryder TB, Wingate VPM, Bailey JA, Lamb CJ. 6.  1986. Differential accumulation of plant defense gene transcripts in a compatible and an incompatible plant-pathogen interaction. Mol. Cell. Biol. 6:1615–23 [Google Scholar]
  7. Bi JL, Felton GW, Murphy JB, Howles PA, Dixon RA, Lamb CJ. 7.  1997. Do plant phenolics confer resistance to specialist and generalist insect herbivores?. J. Food Agric. Chem. 45:4500–4 [Google Scholar]
  8. Borevitz J, Xia Y, Blount JW, Dixon RA, Lamb C. 8.  2000. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–93 [Google Scholar]
  9. Bradley DJ, Kjellbom P, Lamb CJ. 9.  1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30 [Google Scholar]
  10. Brisson LF, Tenhaken R, Lamb C. 10.  1994. Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–12 [Google Scholar]
  11. Cameron RK, Dixon RA, Lamb CJ. 11.  1994. Biologically induced systemic acquired resistance in Arabidopsis thaliana. Plant J. 5:715–25 [Google Scholar]
  12. Chen F, Dixon RA. 12.  2007. Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25:759–61 [Google Scholar]
  13. Corbin DR, Sauer N, Lamb CJ. 13.  1987. Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol. Cell. Biol. 7:4337–44 [Google Scholar]
  14. Cramer CL, Bell JN, Ryder TB, Bailey JA, Schuch W. 14.  et al. 1985. Co-ordinated synthesis of phytoalexin biosynthetic enzymes in biologically-stressed cells of bean (Phaseolus vulgaris L.). EMBO J. 4:285–89 [Google Scholar]
  15. Cramer CL, Edwards K, Dron M, Liang X, Dildine SL. 15.  et al. 1989. Phenylalanine ammonia-lyase gene organization and structure. Plant Mol. Biol. 12:367–83 [Google Scholar]
  16. Cramer CL, Ryder TB, Bell JN, Lamb CJ. 16.  1985. Rapid switching of plant gene expression induced by fungal elicitor. Science 227:1240–43 [Google Scholar]
  17. de Maagd RA, Cameron RK, Dixon RA, Lamb CJ. 17.  1993. Screening methods for Arabidopsis mutants affected in the signal transduction pathways leading to defense responses. Advances in Molecular Genetics of Plant-Microbe Interactions EW Nester, DPS Verma 445–49 Dordrecht, Netherlands: Kluwer Acad. Publ. [Google Scholar]
  18. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K. 18.  et al. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247–50 [Google Scholar]
  19. Delledonne M, Xia Y, Dixon RA, Lamb C. 19.  1998. Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–88The first demonstration of a role for nitric oxide as a signal molecule in induced antimicrobial defenses in plants. [Google Scholar]
  20. Dixon RA, Bendall DS. 20.  1978. Changes in the levels of enzymes of phenylpropanoid and flavonoid synthesis during phaseollin production in cell suspension cultures of Phaseolus vulgaris. Physiol. Plant Pathol. 13:295–306 [Google Scholar]
  21. Dixon RA, Dey PM, Murphy DL, Whitehead IM. 21.  1981. Dose responses for Colletotrichum lindemuthianum elicitor-mediated enzyme induction in French bean cell suspension cultures. Planta 151:272–80 [Google Scholar]
  22. Dixon RA, Gerrish C, Lamb CJ, Robbins MP. 22.  1983. Elicitor modulated induction of chalcone isomerase in Phaseolus vulgaris. Planta 159:561–69 [Google Scholar]
  23. Dixon RA, Harrison MJ, Lamb CJ. 23.  1994. Early events in the activation of plant defense responses. Annu. Rev. Phytopathol. 32:479–501 [Google Scholar]
  24. Dixon RA, Lamb CJ. 24.  1979. Stimulation of de novo synthesis of L-phenylalanine ammonia-lyase in relation to phytoalexin accumulation in Colletotrichum lindemuthianum elicitor-treated cell suspension cultures of French bean (Phaseolus vulgaris). Biochim. Biophys. Acta 586:453–63 [Google Scholar]
  25. Dixon RA, Lamb CJ. 25.  1990. Molecular communication in plant: microbial pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:339–67 [Google Scholar]
  26. Doerner P, Jørgensen JE, You R, Steppuhn J, Lamb C. 26.  1996. Control of root growth and development by cyclin expression. Nature 380:520–23 [Google Scholar]
  27. Doerner PW, Stermer BA, Schmid J, Dixon RA, Lamb CJ. 27.  1990. Plant defense gene promoter-reporter gene fusions in transgenic plants: tools for identification of novel inducers. Bio/Technology 8:845–48 [Google Scholar]
  28. Dröge-Laser W, Kaiser A, Lindsay WP, Halkier B, Loake GA. 28.  et al. 1997. Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP transcription factor, G/HBF-1, in the induction of early transcription-dependent defenses. EMBO J. 16:726–38 [Google Scholar]
  29. Dron M, Clouse SD, Dixon RA, Lawton MA, Lamb CJ. 29.  1988. Glutathione and fungal elicitor regulation of a plant-defense gene promoter in electroporated protoplasts. Proc. Natl. Acad. Sci. USA 85:6738–42 [Google Scholar]
  30. Edwards K, Cramer CL, Schuch W, Lamb CJ, Dixon RA. 30.  1985. Rapid transient induction of phenyl- alanine ammonia-lyase mRNA in elicitor-treated bean cells. Proc. Natl. Acad. Sci. USA 82:6731–35 [Google Scholar]
  31. Elkind Y, Edwards R, Mavandad M, Hedrick SA, Ribak O. 31.  et al. 1990. Abnormal plant development and down regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc. Natl. Acad. Sci. USA 87:9057–61A key publication providing a novel approach for genetically testing the roles of phenylpropanoid compounds in plant defense, and one of the first examples of epigenetic gene silencing in plants. [Google Scholar]
  32. Faktor O, Kooter J, Dixon RA, Lamb CJ. 32.  1996. Functional dissection of a bean chalcone synthase gene promoter in transgenic tobacco plants reveals sequence motifs essential for floral expression. Plant Mol. Biol. 32:845–59 [Google Scholar]
  33. Faktor O, Loake G, Dixon RA, Lamb CJ. 33.  1997. The G-box and H-box in a 39 bp region of a French bean chalcone synthase promoter constitute a tissue-specific regulatory element. Plant J. 11:1105–13 [Google Scholar]
  34. Fan J, Hill L, Crooks C, Doerner P, Lamb C. 34.  2009. Abscisic acid has a key role in modulating diverse plant-pathogen interactions. Plant Physiol. 150:1750–61 [Google Scholar]
  35. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV. 35.  et al. 1999. Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr. Biol. 9:317–20 [Google Scholar]
  36. Filner P, Varner JE. 36.  1967. A test for de novo synthesis of enzymes: density labeling with H2O18 of α-amylase induced by gibberellic acid. Proc. Natl. Acad. Sci. USA 58:1520–26 [Google Scholar]
  37. Hahlbrock K, Lamb CJ, Purwin C, Ebel J, Fautz E, Schäfer E. 37.  1981. Rapid response of suspension-cultured parsley cells to the elicitor from Phytophthora megasperma var. sojae. Plant Physiol. 67:768–73 [Google Scholar]
  38. Harrison MJ, Choudhary AD, Dubery I, Lamb CJ, Dixon RA. 38.  1991. Cis-elements and trans-acting factors for the quantitive expression of a bean chalcone synthase gene promoter in electroporated alfalfa protoplasts. Plant Mol. Biol. 16:877–90 [Google Scholar]
  39. He ZH, Wang ZY, Li JM, Zhu Q, Lamb C. 39.  et al. 2000. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288:2360–63 [Google Scholar]
  40. Hedrick SA, Bell JN, Boller T, Lamb CJ. 40.  1988. Chitinase cDNA cloning and mRNA induction by fungal elicitor, wounding, and infection. Plant Physiol. 86:182–86 [Google Scholar]
  41. Heller W, Hahlbrock K. 41.  1980. Highly purified “flavanone synthase” from parsley catalyzes the formation of naringenin chalcone. Arch. Biochem. Biophys. 200:617–19 [Google Scholar]
  42. Howles PA, Sewalt VJH, Paiva NL, Elkind NL, Bate Y. 42.  et al. 1996. Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol. 112:1617–24 [Google Scholar]
  43. Jacobs M, Rubery PH. 43.  1988. Naturally occurring auxin transport regulators. Science 241:346–49 [Google Scholar]
  44. Keller B, Lamb CJ. 44.  1989. Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes Dev. 3:1639–46 [Google Scholar]
  45. Keller B, Sauer N, Lamb CJ. 45.  1988. Glycine-rich cell wall proteins in bean: gene structure and association of the protein with the vascular system. EMBO J. 7:3625–33 [Google Scholar]
  46. Keller B, Schmid J, Lamb CJ. 46.  1989. Vascular expression of a bean cell wall glycine-rich protein-ß-glucuronidase gene fusion in transgenic tobacco. EMBO J. 8:1309–14 [Google Scholar]
  47. Keller B, Templeton MD, Lamb CJ. 47.  1989. Specific localization of a plant cell wall glycine-rich protein in protoxylem cells of the vascular system. Proc. Natl. Acad. Sci. USA 86:1529–33 [Google Scholar]
  48. Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C. 48.  1997. A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes an intrinsic plasma membrane protein with Ca2+-binding and RanGAP1 domains. Plant Cell 10:255–66 [Google Scholar]
  49. Kreuzaler F, Ragg H, Fautz E, Kuhn DN, Hahlbrock K. 49.  1983. UV-induction of chalcone synthase mRNA in cell suspension cultures of Petroselinum hortense. Proc. Natl. Acad. Sci. USA 80:2591–93 [Google Scholar]
  50. Lamb C, Dixon RA. 50.  1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251–75One of the most highly cited review articles in the plant sciences, providing an in-depth analysis of the generation and role of hydrogen peroxide in defense. [Google Scholar]
  51. Lamb CJ.51.  1977. Phenylalanine ammonia-lyase and cinnamic acid 4-hydroxylase: characterisation of the concomitant changes in enzyme activities in illuminated potato tuber discs. Planta 135:169–75 [Google Scholar]
  52. Lamb CJ.52.  1977. trans-Cinnamic acid as a mediator of the light-stimulated increase in hydroxycinnamoyl-CoA: quinate hydroxycinnamoyl transferase. FEBS Lett. 75:37–39 [Google Scholar]
  53. Lamb CJ.53.  1979. Regulation of enzyme levels in phenylpropanoid biosynthesis: characterization of the modulation by light and pathway intermediates. Arch. Biochem. Biophys. 192:311–17 [Google Scholar]
  54. Lamb CJ.54.  1994. Plant disease resistance genes in signal perception and transduction. Cell 76:419–22 [Google Scholar]
  55. Lamb CJ, Dixon RA. 55.  1978. Stimulation of de novo synthesis of L-phenylalanine ammonia-lyase during induction of phytoalexin biosynthesis in cell suspension cultures of Phaseolus vulgaris. FEBS Lett. 94:277–80 [Google Scholar]
  56. Lamb CJ, Lawton MA, Dron M, Dixon RA. 56.  1989. Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56:215–24 [Google Scholar]
  57. Lamb CJ, Lawton MA, Shields SE. 57.  1981. Density labelling characterisation of the effects of cordycepin and cycloheximide on the turnover of phenylalanine ammonia-lyase. Biochim. Biophys. Acta 675:1–8 [Google Scholar]
  58. Lamb CJ, Merritt TK. 58.  1979. Density labelling studies of the photocontrol of L-phenylalanine ammonia-lyase in discs of potato (Solanum tuberosum) tuber parenchyme. Biochim. Biophys. Acta 588:1–11 [Google Scholar]
  59. Lamb CJ, Merritt TK, Butt VS. 59.  1979. Synthesis and removal of phenylalanine ammonia-lyase activity in illuminated discs of potato tuber parenchyme. Biochim. Biophys. Acta 582:196–212 [Google Scholar]
  60. Lamb CJ, Rubery PH. 60.  1976. Differential effects of cycloheximide on the activity of phenylalanine ammonia-lyase and cinnamic acid 4-hydroxylase in light- and dark-incubated potato tuber discs. Plant Sci. Lett. 7:33–37 [Google Scholar]
  61. Lamb CJ, Rubery PH. 61.  1976. Inhibition of co-operative enzymes by substrate-analogues: possible implications for the physiological significance of negative co-operativity illustrated by phenylalanine metabolism in higher plants. J. Theor. Biol. 60:441–47 [Google Scholar]
  62. Lamb CJ, Rubery PH. 62.  1976. Interpretation of the rate of density labelling of enzymes with 2H2O: possible implications for the mode of action of phytochrome. Biochim. Biophys. Acta 421:308–18 [Google Scholar]
  63. Lamb CJ, Ryals JA, Ward ER, Dixon RA. 63.  1992. Emerging strategies for enhancing crop resistance to microbial pathogens. Bio/Technology 10:1436–45 [Google Scholar]
  64. Lawton MA, Clouse SD, Lamb CJ. 64.  1990. Glutathione-elicited changes in chromatin structure within the promoter of the defense gene chalcone synthase. Plant Cell Rep. 8:561–64 [Google Scholar]
  65. Lawton MA, Dean SJ, Dron M, Kooter JK, Kragh KM, Harrison MJ. 65.  et al. 1991. Silencer region of a chalcone synthase promoter contains multiple binding sites for a factor, SBF-1, closely related to GT-1. Plant Mol. Biol. 16:235–49 [Google Scholar]
  66. Lawton MA, Dixon RA, Hahlbrock K, Lamb CJ. 66.  1983. Rapid induction of phenylalanine ammonia-lyase and of chalcone synthase synthesis in elicitor-treated plant cells. Eur. J. Biochem. 129:593–601 [Google Scholar]
  67. Lawton MA, Dixon RA, Hahlbrock K, Lamb CJ. 67.  1983. Elicitor induction of mRNA activity: rapid effects of elicitor on phenylalanine ammonia-lyase and chalcone synthase mRNA activities in bean cells. Eur. J. Biochem. 130:131–39 [Google Scholar]
  68. Lawton MA, Dixon RA, Lamb CJ. 68.  1980. Elicitor modulation of L-phenylalanine ammonia-lyase in French bean cell suspension cultures. Biochim. Biophys. Acta 633:162–75 [Google Scholar]
  69. Lawton MA, Yamamoto RT, Hanks SK, Lamb CJ. 69.  1989. Molecular cloning of plant transcripts encoding protein kinase homologs. Proc. Natl. Acad. Sci. USA 86:3140–44 [Google Scholar]
  70. Levine A, Tenhaken R, Dixon RA, Lamb CJ. 70.  1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response as a local trigger of programmed cell death and a diffusible inducer of cellular protectant genes. Cell 79:583–93An analysis of the multiple roles of hydrogen peroxide in the HR, emphasizing the importance of a balance between induced cell death and cellular protection mechanisms. [Google Scholar]
  71. Leyva A, Liang X, Pintor-Toro JA, Dixon RA, Lamb CJ. 71.  1992. cis-Element combinations determine phenylalanine ammonia-lyase gene tissue specific expression patterns. Plant Cell 4:263–71 [Google Scholar]
  72. Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ. 72.  1989. Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J. Biol. Chem. 264:14486–92 [Google Scholar]
  73. Liang X, Dron M, Schmid J, Dixon RA, Lamb CJ. 73.  1989. Developmental and environmental regulation of a phenylalanine ammonia-lyase ß-glucuronidase gene fusion in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 86:9284–88 [Google Scholar]
  74. Lindsay WP, Lamb CJ, Dixon RA. 74.  1993. Microbial recognition and activation of plant defense mechanisms. Trends Microbiol. 1:181–86 [Google Scholar]
  75. Lindsay WP, McAlister FM, Zhu Q, He X-Z, Droge-Laser W. 75.  et al. 2002. KAP-2, a protein that binds to the H-box in a bean chalcone synthase promoter, is a novel plant transcription factor with sequence identity to the large subunit of human Ku autoantigen. Plant Mol. Biol. 49:503–14 [Google Scholar]
  76. Loake G, Choudhary AD, Harrison MJ, Mavandad M, Lamb CJ, Dixon RA. 76.  1991. Phenylpropanoid pathway intermediates regulate transient expression of a chalcone synthase gene promoter in electroporated protoplasts. Plant Cell 3:829–40 [Google Scholar]
  77. Loake GJ, Faktor O, Lamb CJ, Dixon RA. 77.  1992. Combination of H-box (CCTACC(N7)CT) and G-box (CACGTG) cis-elements is necessary for feedforward stimulation of a chalcone synthase promoter by the phenylpropanoid pathway intermediate p-coumaric acid. Proc. Natl. Acad. Sci. USA 89:9230–34 [Google Scholar]
  78. Maher EA, Bate NJ, Ni W, Elkind Y, Dixon RA, Lamb CJ. 78.  1994. Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc. Natl. Acad. Sci. USA 91:7802–6An early genetic demonstration of the importance of induced phenylpropanoid compounds in plant disease resistance. [Google Scholar]
  79. Maldonado AM, Dixon RA, Lamb C, Doerner P, Cameron RK. 79.  2002. A putative lipid transfer protein is involved in systemic signaling to establish acquired resistance in Arabidopsis thaliana. Nature 419:399–403Genetic evidence for the role of a lipid transfer protein (and therefore possibly oxylipin signal molecules) in long distance signal transduction to establish SAR. [Google Scholar]
  80. Mehdy MC, Lamb CJ. 80.  1987. Chalcone isomerase cDNA cloning and mRNA induction by fungal elicitor, wounding and infection. EMBO J. 6:1527–33 [Google Scholar]
  81. Moon J, Parry G, Estelle M. 81.  2004. The ubiquitin-proteasome pathway and plant development. Plant Cell 16:3181–95 [Google Scholar]
  82. Napoli C, Lemieux C, Jorgensen R. 82.  1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–89 [Google Scholar]
  83. Niggeweg R, Michael AJ, Martin C. 83.  2004. Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 22:746–54 [Google Scholar]
  84. O'Connell RJ, Bailey JA, Vose IR, Lamb CJ. 84.  1986. Immunogold labelling of fungal antigens in cells of Phaseolus vulgaris infected by Colletotrichum lindemuthianum. Physiol. Mol. Plant Pathol. 28:99–105 [Google Scholar]
  85. Ohl S, Hedrick SA, Chory J, Lamb CJ. 85.  1990. Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 2:837–48 [Google Scholar]
  86. Pallas JA, Paiva NL, Lamb CJ, Dixon RA. 86.  1996. Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10:281–93 [Google Scholar]
  87. Rubery PH, Northcote DH. 87.  1968. Site of phenylalanine ammonia-lyase activity and synthesis of lignin during xylem differentiation. Nature 219:1230–34 [Google Scholar]
  88. Ryder TB, Cramer CL, Bell JN, Robbins MP, Dixon RA, Lamb CJ. 88.  1984. Elicitor rapidly induces chalcone synthase mRNA in Phaseolus vulgaris cells at the onset of the phytoalexin response. Proc. Natl. Acad. Sci. USA 81:5724–28 [Google Scholar]
  89. Ryder TB, Hedrick SA, Bell JN, Liang X, Clouse SD, Lamb CJ. 89.  1987. Organization and differential activation of a gene family encoding the plant defense enzyme chalcone synthase in Phaseolus vulgaris. Mol. Gen. Genet. 210:219–33 [Google Scholar]
  90. Sauer N, Corbin DR, Keller B, Lamb CJ. 90.  1990. Cloning and characterization of a wound-specific hydroxyproline-rich glycoprotein in Phaseolus vulgaris. Plant Cell Environ. 13:257–66 [Google Scholar]
  91. Schmid J, Doerner PW, Clouse SD, Dixon RA, Lamb CJ. 91.  1990. Developmental and environmental regulation of a bean chalcone synthase promoter in transgenic tobacco. Plant Cell 2:619–31 [Google Scholar]
  92. Schröder J, Kreuzaler F, Schäfer E, Hahlbrock K. 92.  1979. Concomitant induction of phenylalanine ammonia-lyase and flavanone synthase mRNAs in irradiated plant cells. J. Biol. Chem. 254:57–65 [Google Scholar]
  93. Seguin A, Laible G, Leyva A, Dixon RA, Lamb CJ. 93.  1997. Characterization of a gene encoding a DNA-binding protein that interacts with vascular specific cis-elements of the phenylalanine ammonia-lyase promoter. Plant Mol. Biol. 35:281–91 [Google Scholar]
  94. Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA, Lamb CJ. 94.  1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9:261–70Evidence that salicylic acid acts in an amplification loop during transduction of pathogen signals for induced defense responses. [Google Scholar]
  95. Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner JE, Lamb CJ. 95.  1985. Accumulation of hydroxyproline-rich glycoprotein mRNAs in response to fungal elicitor and infection. Proc. Natl. Acad. Sci. USA 82:6551–55 [Google Scholar]
  96. Templeton MD, Dixon RA, Lamb CJ, Lawton MA. 96.  1990. Hydroxyproline-rich glycoprotein transcripts exhibit different spatial patterns of accumulation in compatible and incompatible interactions between Phaseolus vulgaris and Colletotrichum lindemuthianum. Plant Physiol. 94:1265–69 [Google Scholar]
  97. Tenhaken R, Levine A, Brisson LF, Dixon RA, Lamb CJ. 97.  1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. USA 92:4158–63 [Google Scholar]
  98. Vierstra RD.98.  1993. Protein degradation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:385–410 [Google Scholar]
  99. Weigel D, Ahn JH, Blazquez MA, Borewitz J, Christensen SK. 99.  et al. 2000. Activation tagging in Arabidopsis. Plant Physiol. 122:1003–13 [Google Scholar]
  100. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 100.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  101. Wingate VPM, Lawton MA, Lamb CJ. 101.  1988. Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol. 87:206–10 [Google Scholar]
  102. Xia Y, Suzuki H, Borevitz J, Blount JW, Guo Z. 102.  et al. 2003. An extracellular aspartic protease mediates disease resistance in Arabidopsis. EMBO J. 23:980–88Genetic evidence of a key role for host-associated proteolytic reaction as an early step in defense gene induction by pathogen signals. [Google Scholar]
  103. Zhu Q, Chappell J, Hedrick SA, Lamb CJ. 103.  1995. Accurate in vitro transcription from circularized plasmid templates by plant whole cell extracts. Plant J. 7:1021–30 [Google Scholar]
  104. Zhu Q, Dabi T, Lamb C. 104.  1995. TATA box and initiator functions in the accurate transcription of a plant minimal promoter in vitro. Plant Cell 7:1681–89 [Google Scholar]
  105. Zhu Q, Maher EA, Masoud S, Dixon RA, Lamb CJ. 105.  1994. Enhanced protection against fungal attack by constitutive co-expression of chitinase and glucanase genes in transgenic tobacco. Bio/Technology 12:807–12 [Google Scholar]
/content/journals/10.1146/annurev-phyto-072910-095224
Loading
/content/journals/10.1146/annurev-phyto-072910-095224
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error