Differential Expression of Pine and Cronartium quercuum f. sp. fusiforme Genes in Fusiform Rust Galls

Applied and Environmental Microbiology

Volumn 70, Issue 1, 2004, Pages 441-451

  Warren, Jaimie M ^a,c   Covert, Sarah F ^b  

^a University of Georgia ^*  (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c Ushas Inc Immunity Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLONING; DNA; GENES; RNA; TISSUE;

GENE EXPRESSIONS;

MICROBIOLOGY;

COMPLEMENTARY DNA; RIBOSOME RNA; RNA;

ARTICLE; CONTROLLED STUDY; CRONARTIUM QUERCUUM; FUNGUS; FUNGUS CULTURE; GENE EXPRESSION; GENE IDENTIFICATION; GENE ISOLATION; HYBRIDIZATION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PINE; PLANT DEFENSE; PLANT DEVELOPMENT; PLANT STEM; PLANT TISSUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS;

BASIDIOMYCOTA; DNA, COMPLEMENTARY; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; PINUS; PINUS TAEDA; PLANT PROTEINS; PLANT TUMORS; QUERCUS; TRANSCRIPTION, GENETIC;

CRONARTIUM; CRONARTIUM QUERCUUM F. SP. FUSIFORME; FUNGI; PINUS ECHINATA;

EID: 0345868873     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.1.441-451.2004     Document Type: Article

References (90)

1. Albert, B., D. Bray, J. Lewis, M. Raff, K. Roberts, and J. D. Watson (ed.). 1994. Molecular biology of the cell, 3rd ed. Garland Publishing Inc., New York, N. Y.
2. Alexopoulos, C. J., C. W. Mims, and M. Blackwell (ed.). 1996. Introductory mycology, 4th ed. John Wiley & Sons, Inc., New York, N.Y.
3. Aligue, R., H. Akhavanniak, and P. Russell. 1994. A role of Hsp90 in cell cycle control: Weel tyrosine kinase activity requires interaction with Hsp90. EMBO J. 13:6099-6106.
4. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. H. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
5. Amerson, H. V., and R. L. Mott. 1972. Technique for axenic production and application of Cronartium fusiforme basidiospores. Phytopathology 68:673-675.
6. Anderson, R. L., J. P. McClure, N. Cost, and R. J. Uhler. 1986. Estimating fusiform rust losses in five southeast states. South. J. Appl. Forest. 10:237-240.
7. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1998. Current protocols in molecular biology, vol. 1. John Wiley and Sons Inc., New York, N.Y.
8. Benito, E. P., A. ten Have, J. W. van't Klooster, and J. A. L. van Kan. 1998. Fungal and plant gene expression during synchronized infection of tomato leaves by Botryis cinerea. Eur. J. Plant Pathol. 104:207-220.
9. Benito, E. P., T. Prins, and J. A. L. van Kan. 1996. Application of differential display RT-PCR to the analysis of gene expression in a plant-fungus interaction. Plant Mol. Biol. 32:947-957.
10. Black, S. D., and M. J. Coon. 1982. Structural features of liver microsomal NADPH-cytochrome P-450 reductase-hydrophobic domain, hydrophilic domain, and connecting region. J. Biol. Chem. 257:5929-5938.
11. Caplan, A. J. 1999. Hsp90's secrets unfold: new insights from structural and functional studies. Trends Cell Biol. 9:262-268.
12. Chang, S., J. Puryear, and J. Cairney. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11:113-116.
13. Clark, S. E., M. P. Running, and E. M. Meyerowitz. 1993. Clavata 1, a regulator of meristem and flower development in Arabidopsis. Development 119:397-418.
14. Cubbage, F. W., J. M. Pye, T. P. Holmes, and J. E. Wagner. 2000. An economic evaluation of fusiform rust protection research. South. J. Appl. Forest. 24:77-85.
15. Cyr, R. J. 1994. Microtubules in plant morphogenesis-role of the cortical array. Annu. Rev. Cell Biol. 10:153-180.
16. Dal Degan, F., B. Ribadeau-Dumas, and K. Breddam. 1992. Purification and characterization of two serine carboxypeptidases from Aspergillus niger and their use in C-terminal sequencing of proteins and peptide synthesis. Appl. Environ. Microbiol. 58:2144-2152.
17. Diaz, E. C., D. Tagu, and F. Martin. 1997. Ribosomal DNA internal transcribed spacers to estimate the proportion of Pisolithus tinctorius and Eucalyptus globulus RNAs in ectomycorrhiza. Appl. Environ. Microbiol. 63:840-843.
18. Ditt, R. F., E. W. Nester, and L. Comai. 2001. Plant gene expression response to Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 98:10954-10959.
19. Duina, A. A., J. C. Hui-Chen, J. A. Marsc, S. Lindquist, and R. F. Gaber. 1996. A cyclophilin function in HSP90-dependent signal transduction. Science 274:1713-1715.
20. Feuillet, C., G. Schachermayr, and B. Keller. 1997. Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J. 11:45-52.
21. Fletcher, J. C., and E. M. Meyerowitz. 2000. Cell signaling within the shoot meristem. Curr. Opin. Plant Biol. 3:23-30.
22. Freskgard, P. O., N. Bergenhem, B. H. Jonsson, M. Svensson, and U. Carlsson. 1992. Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258:466-468.
23. Garcia-Olmedo, F., A. Molina, A. Segura, and M. Moreno. 1995. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol. 3:72-74.
24. George, H. L., K. D. Hirschi, and H. D. VanEtten. 1998. Biochemical properties of the products of cytochrome P450 genes (PDA) encoding pisatin demethylase activity in Nectria haematococca. Arch. Microbiol. 170:147-154.
25. Godoy, A. V., A. S. Lazzaro, C. A. Casalongue, and B. San Segundo. 2000. Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions. Plant Sci. 152:123-134.
26. Gonzalez, F. J., and D. W. Nebert. 1990. Evolution of the P450 gene superfamily-animal plant warfare, molecular drive and human genetic-differences in drug oxidation. Trends Genet. 6:182-186.
27. Goodard, R. H., S. M. Wick, C. D. Silflow, and D. P. Snustad. 1994. Microtubule components of the plant cell cytoskeleton. Plant Physiol. 104:1-6.
28. Gray, D. J., H. V. Amerson, and C. G. Van Dyke. 1982. An ultrastructural comparison of monokaryotic and dikaryotic haustoria formed by the fusiform rust fungus Cronartium quercuum f. sp. fusiforme. Can. J. Bot. 60:2914-2922.
29. Gundersen, G. G., and T. A. Cook. 1999. Microtubules and signal transduction. Curr. Opin. Cell Biol. 11:81-94.
30. Hahn, M., and K. Mendgen. 1992. Isolation by ConA binding of haustoria from different rust fungi and comparison of their surface qualities. Protoplasma 170:95-103.
31. Hahn, M., and K. Mendgen. 1997. Characterization of in planta-induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant Microbe Interact. 10:427-437.
32. Hahn, M., and K. Mendgen. 2001. Signal and nutrient exchange at biotrophic plant-fungus interfaces. Curr. Opin. Plant Biol. 4:322-327.
33. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:40-52.
34. Hare, R. C. 1978. Axenic culture of Cronartium fusiforme from three spore forms. Can. J. Bot. 56:2641-2647.
35. Heath, M. C. 1997. Signaling between pathogenic rust fungi and resistant or susceptible host plants. Ann. Bot. 80:713-720.
36. Hollis, C. A., R. A. Schmidt, and J. W. Kimbrough. 1972. Axenic culture of Cronartium fusiforme. Phytopathology 62:1417-1419.
37. Hu, A., and H. V. Amerson. 1991. Single genotype axenic cultures of Cronartium quercuum f. sp. fusiforme. Phytopathology 81:1294-1297.
38. Hu, A., H. V. Amerson, and L. J. J. R. Frampton. 1994. Isolation and growth of single genotype axenic cultures of Cronartium quercuum f. sp. fusiforme using hyphal fragments from multi-genotype stock colonies. New Forests 8:299-308.
39. Hussey, P. J., D. P. Snustad, and C. D. Silflow. 1991. Tubulin gene expression in higher plants, p. 15-27. In C. W. Lloyd (ed.), The cytoskeletal basis of plant growth and form. Academic Press, London, United Kingdom.
40. Jackson, L. W. R., and J. N. Parker. 1958. Anatomy of fusiform rust galls on loblolly pine. Phytopathology 48:637-640.
41. Jewell, F. F., R. P. True, and S. L. Mallett. 1962. Histology of Cronartium in slash pine seedlings. Phytopathology 52:850-858.
42. Jinn, T.-L., J. M. Stone, and J. C. Walker. 2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 14:108-117.
43. Johnston, R. F., S. C. Pickett, and D. L. Barker. 1990. Autoradiography using storage phosphor technology. Electrophoresis 11:355-360.
44. Jones, L. J., S. T. Yue, C. Y. Cheung, and V. L. Singer. 1998. RNA quantitation by fluorescence-based solution assay: RiboGreen reagent characterization. Anal. Biochem. 265:368-374.
45. Kapulnik, Y., H. Volpin, H. Itzhaki, D. Ganon, S. Galili, R. David, O. Shaul, Y. Elad, I. Chet, and Y. Okon. 1996. Suppression of defence responses in mycorrhizal alfalfa and tobacco roots. New Phytol. 133:59-64.
46. Komjanc, M., S. Festi, L. Rizzotti, L. Cattivelli, F. Cervone, and G. De Lorenzo. 1999. A leucine-rich repeat receptor-like protein kinase (LRPKm1) gene induced in Malus x domestica by Venturia inaequalis infection and salicylic acid treatment. Plant Mol. Biol. 40:945-957.
47. Kretzer, A. M., and T. D. Bruns. 1999. Use of atp6 in fungal phylogenetics: an example from the Boletales. Mol. Phylogenet. Evol. 13:483-492.
48. Lambais, M. R., and M. C. Mehdy. 1993. Suppression of endochitinase, beta-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol. Plant-Microbe Interact. 6:75-83.
49. Lange, J., Z.-P. Xie, W. J. Broughton, R. Vogeli-Lange, and T. Boller. 1999. A gene encoding a receptor-like protein kinase in the roots of common bean is differentially regulated in response to pathogens, symbionts and nodulation factors. Plant Sci. 142:133-145.
50. Lapopin, L., V. Gianinazzi-Pearson, and P. Franken. 1999. Comparative differential RNA display analysis of arbuscular mycorrhiza in Pisum sativum wild type and a mutant defective in late stage development. Plant Mol. Biol. 41:669-677.
51. Liang, P., L. Averboukh, and A. B. Pardee. 1993. Distribution and cloning of eukaryotic mRNAs by means of differential display: refinements and optimization. Nucleic Acids Res. 21:3269-3275.
52. Mahe, A., J. Grisvard, and M. Dron. 1992. Fungal- and plant-specific gene markers to follow the bean anthracnose infection process and normalize a bean chitinase mRNA induction. Mol. Plant-Microbe Interact. 5:242-248.
53. Maldonado-Mendoza, I. E., G. R. Dewbre, M. L. van Buuren, W. K. Versaw, and M. J. Harrison. 2002. Methods to estimate the proportion of plant and fungal RNA in an arbuscular mycorrhiza. Mycorrhiza 12:67-74.
54. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
55. Martin-Laurent, F., D. van Tuinen, E. Dumas-Gaudot, V. Gianinazzi-Pearson, S. Gianinazzi, and P. Franken. 1997. Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosis-regulated plant gene. Mol. Gen. Genet. 256:37-44.
56. McHenry, J. Z., J. T. Christeller, E. A. Slade, and W. A. Laing. 1996. The major extracellular proteinases of the silverleaf fungus, Chondrostereum purpureum, are metalloproteinases. Plant Pathol. 45:552-563.
57. Mellersh, D. G., and M. C. Heath. 2001. Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13:413-424.
58. Molina, A., and F. Garcia-Olmedo. 1993. Developmental and pathogen-induced expression of three barley genes encoding lipid transfer proteins. Plant J. 4:983-991.
59. Molina, A., and F. Garica-Olmedo. 1997. Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J. 12:669-675.
60. Montoliu, L., J. Rigau, and P. Puigdomenech. 1989. A tandem of alpha-tubulin genes preferentially expressed in radicular tissues from Zea mays. Plant Mol. Biol. 14:1-15.
61. Paquin, B., M.-J. Laforest, L. Forget, I. Roewer, Z. Wang, J. Longcore, and B. F. Lang. 1997. The fungal mitochondrial genome project: evolution of fungal mitochondrial genomes and their gene expression. Curr. Genet. 31:380-395.
62. Pavlukova, E. B., M. A. Belozersky, and Y. E. Dunaevsky. 1998. Extracellular proteolytic enzymes of filamentous fungi. Biochemistry (Moscow) 63:899-928.
63. Perfect, S. E., R. J. O'Connell, E. F. Green, C. Doering-Saad, and J. R. Green. 1998. Expression of a fungal proline-rich glycoprotein specific to the biotrophic interface formed in the Colletotrichum-bean interaction. Plant J. 15:273-279.
64. Rowan, S. J. 1970. Fusiform rust gall formation and cytokinin of loblolly pine. Phytopathology 60:1225-1226.
65. Sabala, I., M. Elfstrand, D. Clapham, and S. von Arnold. 2000. Tissue-specific expression of Pal8, a putative lipid transfer protein gene, during embryo development in Norway spruce (Picea abies). Plant Mol. Biol. 42:461-478.
66. Schmid, F. X., L. M. Mayr, M. Mucke, and E. R. Schonbrunner. 1993. Prolyl isomerases: role in protein folding. Adv. Protein Chem. 44:25-66.
67. Seifers, D., V. Ammon, and J. Spencer. 1985. Alteration in auxin levels in selected southern pines inoculated with the fusiform rust fungus. Agric. Ecosys. Environ. 14:131-138.
68. Shirley, B. W., and R. B. Meagher. 1990. A potential role for RNA turnover in the light regulation of plant gene expression: ribulose-1,5-bisphosphate carboxylase small subunit in soybean. Nucleic Acids Res. 18:3377-3385.
69. Sikorski, M. M., J. Biesiadka, A. E. Kasperska, J. Kopcinska, B. Lotocka, W. Golinowski, and A. B. Legocki. 1999. Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci. 149:125-137.
70. Singer, V. L., L. J. Jones, S. T. Yue, and R. P. Haugland. 1997. Characterization of PicoGreen reagent and development of a fluorescence-based solution assay for double-stranded DNA quantitation. Anal. Biochem. 249:228-238.
71. Song, W.-Y., L.-Y. Pi, G.-L. Wang, J. Gardner, T. Hoisten, and P. C. Ronald. 1997. Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279-1287.
72. Stein, J. C., B. Howlett, D. C. Boyes, M. E. Nasrallah, and J. B. Nasrallah. 1991. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. USA 88:8816-8820.
73. Stephenson, S. A., J. Hatfield, A. G. Rusu, D. J. Maclean, and J. M. Manners. 2000. CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol. Plant-Microbe Interact. 13:929-941.
74. St. Leger, R. J. 1995. The role of cuticle-degrading proteases in fungal pathogenesis of insects. Can. J. Bot. 73:S1119-S1125.
75. Stocker, M., J. Garcia-Mas, P. Arus, R. Messeguer, and P. Puigdomenech. 1993. A highly conserved alpha-tubulin sequence from Prunus amyedalus. Plant Mol. Biol. 22:913-916.
76. Tainter, F. H., and R. L. Anderson. 1993. Twenty-six new pine hosts of fusiform rusts. Plant Dis. 77:17-20.
77. Thompson, D. M., and R. B. Meagher. 1990. Transcriptional and posttranscriptional processes regulate expression of RNA encoding the small subunit of ribulose-1,5-biphosphate carboxylase differently in petunia and in soybean. Nucleic Acids Res. 18:3621-3629.
78. Uribe, X., M. A. Torres, M. Capellades, P. Puigdomenech, and J. Rigau. 1998. Maize alpha-tubulin genes are expressed according to specific patterns of cell differentiation. Plant Mol. Biol. 37:1069-1078.
79. van den Hombergh, J. P. T. W., G. Jarai, F. P. Buxton, and J. Visser. 1994. Cloning, characterization and expression of pepF, a gene coding a serine carboxypeptidase from Aspergillus niger. Gene 151:73-79.
80. Viterbo, A., B. Yagen, and A. M. Mayer. 1993. Cucurbitacins, attack enzymes and laccase in Botrytis cinerea. Phytochemistry 32:61-65.
81. Voegele, R. T., C. Struck, M. Hahn, and K. Mendgen. 2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromycesfabae. Proc. Natl. Acad. Sci. USA 98:8133-8138.
82. Vogeli-Lange, R., N. Burckert, T. Boller, and A. Wiemken. 1996. Rapid selection and classification of positive clones generated by mRNA differential display. Nucleic Acids Res. 24:1385-1386.
83. Wagner, D. B., G. T. Furnier, M. A. Saghai-Maroof, S. M. Williams, B. P. Dancik, and R. W. Allard. 1987. Chloroplast DNA polymorphisms in lodge-pole and jack pines and their hybrids. Proc. Natl. Acad. Sci. USA 84:2097-2100.
84. Walker, J. C. 1993. Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J. 3:451-456.
85. Warth, R., P.-A. Briand, and D. Picard. 1997. Functional analysis of the yeast 40 kDa cyclophilin Cyp40 and its role for viability and steroid receptor regulation. Biol. Chem. 278:381-391.
86. Waspi, U., P. Schweizer, and R. Dudler. 2001. Syringolin reprograms wheat to undergo hypersensitive cell death in a compatible interaction with powdery mildew. Plant Cell 13:153-161.
87. Wendland, J., K. B. Lengeler, and E. Kothe. 1996. An instant preparation method for nucleic acids of filamentous fungi. Fungal Genet. News 43:54-55.
88. Yabusaki, Y., H. Murakami, and H. Ohkawa. 1988. Primary structure of Saccharomyces cerevisiae NADPH-cytochrome P450 reductase deduced from nucleotide sequence of its cloned gene. J. Biochem. 103:1004-1010.
89. Zhang, M. Y., and C. Y. Liang. 2000. Progress in the studies of lipid-transfer protein. Prog. Biochem. Biophys. 27:244-247.
90. Zugel, U., and S. H. E. Kaufmann. 1999. Role of heat shock proteins in protection from and pathogenesis of infectious diseases. Clin. Microbiol. Rev. 12:19-39.