Endogenous overexpression of Populus MYB186 increases trichome density, improves insect pest resistance, and impacts plant growth

Plant Journal

Volumn 64, Issue 3, 2010, Pages 419-432

  Plett, Jonathan M ^a   Wilkins, Olivia ^b   Campbell, Malcolm M ^b,c   Ralph, Steven G ^d   Regan, Sharon ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Activation tagging; Growth rate; Herbivory; Poplar; R2R3 MYB; Trichome

Indexed keywords

ACTIVATION TAGGING; HERBIVORY; POPLAR; R2R3-MYB; TRICHOME;

GENE EXPRESSION; GENE EXPRESSION REGULATION; GROWTH RATE;

GENE ENCODING;

PLANT RNA; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; ASPEN; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOTH; MUTATION; PHENOTYPE; PHOTOSYNTHESIS; PLANT EPIDERMIS; PLANT GENE;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MOTHS; MUTAGENESIS, INSERTIONAL; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PHOTOSYNTHESIS; PLANT EPIDERMIS; PLANT PROTEINS; POPULUS; RNA, PLANT;

ARABIDOPSIS; ARABIDOPSIS THALIANA; HEXAPODA; LEPIDOPTERA; ORGYIA LEUCOSTIGMA; ORGYIA THYELLINA; POPULUS; POPULUS ALBA; POPULUS TREMULA;

EID: 78149445826     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04343.x     Document Type: Article

References (80)

1. agren, J., and, Schemske, D.W., (1993) The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am. Nat. 141, 338-350.
2. 2 New Phytol. 165, 351-371.
3. Avila, J., Nieto, C., Canas, L., Benito, M.J., and, Paz-Ares, J., (1993) Petunia hybrid genes related to the maize regulatory C1 gene and to animal myb proto-oncogenes. Plant J. 3, 553-562.
4. Benjamini, Y., and, Hochberg, Y., (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
5. Benz, B.W., and, Martin, C.E., (2006) Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). J. Plant Physiol. 163, 648-656.
6. Benzing, D.H., (1976) Bromeliad trichomes: structure, function and ecological significance. Selbryana 1, 330-348.
7. Benzing, D.H., and, Renfrow, A., (1971) The significance of photosynthetic efficiency to habitat preference and phylogeny among Tillandsioid Bromeliads. Bot. Gaz. 132, 19-30.
8. Benzing, D.H., Henderson, K., Kessel, B., and, Sulak, J., (1976) The absorptive capacities of Bromeliad trichomes. Am. J. Bot. 63, 1009-1014.
9. Billings, W.D., and, Morris, R.J., (1951) Reflection of visible and infrared radiation from leaves of different ecological groups. Am. J. Bot. 38, 327-331.
10. Bodnaryk, R.P., (1996) Physical and chemical defenses of pods and seeds of white mustard (Sinapis alba L.) against tarnished plant bugs Lygus lineolaris (Palisor de Baeuvois) (Heteroptera: Miridae). Can. J. Plant Sci. 76, 33-36.
11. Boeger, M.R.T., Alves, L.C., and, Negrelle, R.R.B., (2004) Leaf morphology of 89 tree species from a lowland tropical rain forest (Atlantic Forest) in south Brazil. Braz. Arch. Biol. Technol. 47, 933-943.
12. Brewer, C.A., and, Smith, W.K., (1994) Influence of simulated dewfall on photosynthesis and yield in soybean isolines (glycine max [L.] Merr. CV Williams) with different trichome densities. Int. J. Plant Sci. 155, 460-466.
13. Choinski, J.S., and, Wise, R.R., (1999) Leaf growth and development in relation to gas exchange in Querus marilandica Muenchh. J. Plant Physiol. 154, 302-309.
14. Dillen, S.Y., Marron, N., Kock, B., and, Ceulemans, R., (2008) Genetic variation of stomatal traits and carbon isotope discrimination in two hybrid poplar families (Populus deltoidsS9-2 x P. nigraGhoy and P. deltoidsS9-2 x P. trichocarpaV24. Ann. Bot. 102, 399-407.
15. Downes, B.P., Stupar, R.M., Gingerich, D.J., and, Vierstra, R.D., (2003) The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J. 35, 729-742.
16. 2? Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 609-639.
17. Ehleringer, J.R., BjArkman, O., and, Mooney, H.A., (1976) Leaf pubescence: effects on absorptance and photosynthesis in a desert shrub. Science, 192, 376-377.
18. El Refy, A.E., Perazza, D., Zekraoui, L., Valay, J., Bechtold, N., Brown, S., Hülskamp, M., Herzog, M., and, Bonneville, J.M., (2004) The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol. Genet. Genomics, 270, 403-414.
19. Eller, B.M., and, Willi, P., (1977) The significance of leaf pubescence for the absorption of global radiation by Tussilago farfara L. Oecologia, 29, 179-187.
20. Espigares, T., and, Peco, B., (1995) Mediterranean annual pasture dynamics: impact of autumn drought. J. Ecol. 83, 135-142.
21. Ferris, R., Long, L., Bunn, S.M., Robinson, K.M., Bradshaw, H.D., Rae, A.M., and, Taylor, G., (2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol. 22, 633-640.
22. Folkers, U., Berger, J., and, Hülskamp, M., (1997) Cell morphogenesis of trichomes in Arabidopsis: differential regulation of primary and secondary branching by branch initiation regulators and cell size. Development, 124, 3779-3786.
23. Fordyce, J.A., and, Agrawal, A., (2001) The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. J. Anim. Ecol. 70, 997-1005.
24. Gausman, H.W., and, Cardenas, R., (1969) Effect of leaf pubescence of Gynura aurantiaca on light reflectance. Bot. Gaz. 130, 158-162.
25. Gausman, H.W., and, Cardenas, R., (1973) Light reflectance by leaflets of pubescent, normal, and glabrous soybean lines. Agron. J. 65, 837-838.
26. Gautier, L., Cope, L., Bolstad, B.M., and, Irizarry, R.A., (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics, 20, 307-315.
27. Gentleman, R.C., Carey, V.J., Bates, D.M., etal. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Bio. 5, R80.
28. Gentleman, R.C., Carey, V.J., Huber, W., and, Hahne, F., (2009) Genefilter: methods for filtering genes from microarray experiments. R Package Version 1.24.2.
29. Glover, B.J., Perez-Rodriguez, M., and, Martin, C., (1998) Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development, 125, 3509-3519.
30. Gruber, M., Wang, S., Ethier, S., Holowachuk, J., Bonham-Smith, P., Soroka, J., and, Lloyd, A., (2006) "HAIRY CANOLA"Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol. Biol. 60, 679-698.
31. Harrison, E.J., Bush, M., Plett, J.M., etal. (2007) Diverse developmental mutants revealed in an activation-tagged population of poplar. Can. J. Bot. 85, 1071-1081.
32. Ishida, T., Kurata, T., Okada, K., and, Wada, T., (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59, 365-386.
33. Jakoby, M.J., Falkenhan, D., Mader, M.T., Brininstool, G., Wischnitzki, E., Platz, N., Hudson, A., Hulskamp, M., Larkin, J., and, Schnittger, A., (2008) Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol. 148, 1583-1602.
34. Jin, H., and, Martin, C., (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol. Biol. 41, 577-585.
35. Jin, H.L., Cominelli, E., Bailey, P., Parr, A., Mehrtens, F., Jones, J., Tonelli, C., Weisshaar, B., and, Martin, C., (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J. 19, 6150-6161.
36. Kazama, H., Dan, H., Imaseki, H., and, Wasteneys, J.O., (2004) Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiol. 134, 1614-1623.
37. Kenzo, T., Yoneda, R., Azani, M.A., and, Majid, N.M., (2008) Changes in leaf water use after removal of leaf lower surface hairs on Mallotus macrostachyus (Euphorbiaceae) in a tropical secondary forest in Malaysia. J. For. Res. 13, 137-142.
38. Kirik, V., Schnittger, A., Radchuk, V., Adler, K., Hulskamp, M., and, Baumlein, H., (2001) Ectopic expression of the Arabidopsis AtMYB23 gene induces differentiation of trichome cells. Dev. Biol. 235, 366-377.
39. Kirik, V., Lee, M.M., Wester, K., Herrmann, U., Zheng, Z., Oppenheimer, D., Schiefelbein, J., and, Hulskamp, M., (2005) Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development, 132, 1477-1485.
40. Kivimäki, M., Karkkainen, K., Gaudeul, M., Loe, G., and, Argen, J., (2007) Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata. Mol. Ecol. 16, 453-462.
41. Kranz, H.D., Denekamp, M., Greco, R., etal. (1998) Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16, 263-276.
42. Levin, D., (1973) The role of trichomes in plant defense. Q. Rev. Biol. 48, 3-15.
43. 2 world. Glob. Change Biol. 12, 1094-1106.
44. Lieckfeldt, E., Simon-Rosin, U., Kose, F., Zoeller, D., Schliep, M., and, Fisahn, J., (2008) Gene expression profiling of single epidermal, basal and trichome cells of Arabidopsis thaliana. J. Plant Physiol. 165, 1530-1544.
45. Marks, M.D., Wenger, J.P., Gilding, E., Jilk, R., and, Dixon, R.A., (2009) Transcriptome analysis of Arabidopsis wild-type and gl3-sst sim trichomes identifies four additional genes required for trichome development. Mol. Plant, 2, 803-822.
46. Martin, C.E., and, Schmitt, A.K., (1989) Unusual water relations in the cam atmospheric epiphyte Tillandsia usneoides L. (Bromeliaceae). Bot. Gaz. 150, 1-8.
47. Mauricio, R., (1998) Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana. Am. Nat. 151, 20-28.
48. McCarthy, D.J., and, Smyth, G.K., (2009) Testing significance relative to a fold-change threshold is a TREAT. Bioinformatics, 25, 765-771.
49. Meissner, R.C., Jin, H., Cominelli, E., etal. (1999) Function search in a large transcription factor gene family in Arabidopsis: assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Plant Cell, 11, 1827-1840.
50. Myneni, R.B., Hall, F.G., Sellers, P.J., and, Marshak, A.L., (1995) The interpretation of spectral vegetation indexes. IEEE Trans. Geosci. Remote Sens. 33, 481-486.
51. Neal, J.J., Steffens, J.C., and, Tingey, W.M., (1989) Glandular trichomes of Solanum berhaultii and resistance to the Colorado potato beetle. Ent. Exp. Appl. 51, 133-140.
52. Noda, K., Glover, B.J., Linstead, P., and, Martin, C., (1994) Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature, 369, 661-664.
53. Norby, R.J., Wullschleger, S.D., Gunderson, C.A., Johnson, D.W., and, Ceulemans, R., (1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant Cell Environ. 22, 683-714.
54. 2do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol. 162, 253-280.
55. Oppenheimer, D.G., Herman, P.L., Sivakumaran, S., Esch, J., and, Marks, M.D., (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell, 67, 483-493.
56. Payne, T., Clement, J., Arnold, D., and, Lloyd, A., (1999) Heterologous myb genes distinct from GL1 enhance trichome production when overexpressed in Nicotiana tabacum. Development, 126, 671-682.
57. Pearman, G.I., (1966) The reflection of visible radiation from leaves of some Western Australian species. Aust. J. Biol. Sci. 19, 97-103.
58. Perazza, D., Herzog, M., Hulskamp, M., Brown, S., Dorne, A.M., and, Bonneville, J.M., (1999) Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics, 152, 461-476.
59. 2 increases photosynthesis, biomass and productivity, and modifies gene expression in sugarcane. Plant Cell Environ. 31, 1116-1127.
60. Perez-Estrada, L.B., Cano-Santana, Z., and, Oyama, K., (2000) Variation in leaf trichomes of Wigandia urens: environmental factors and physiological consequences. Tree Physiol. 20, 629-632.
61. Plett, J.M., Mathur, J., and, Regan, S., (2009) Ethylene receptor ETR2 controls trichome branching by regulating cytoskeleton assembly in Arabidopsis. J. Exp. Bot. 60, 3923-3933.
62. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. In.Vienna, Austria: R Foundation for Statistical Computing.
63. Rhee, S.Y., Beavis, W., Berardini, T.Z., etal. (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31, 224-228.
64. Riechmann, J.L., Heard, J., Martin, G., etal. (2000) Arabidopsis transcription factors: Genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
65. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jürgens, G., and, Hülskamp, M., (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21, 5036-5046.
66. Schreuder, M.D.J., Brewer, C.A., and, Heine, C., (2001) Modeled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. J. Theor. Biol. 210, 23-32.
67. Sellers, P.J., (1985) Canopy reflectance, photosynthesis, and transpiration. Int. J. Remote Sens. 6, 1335-1372.
68. Shangguan, X.-X., Xu, B., Yu, Z.-X., Wang, L.-J., and, Chen, X.-Y., (2008) Promoter of a cotton fibre MYB gene functional in trichomes of Arabidopsis and glandular trichomes in tobacco. J. Exp. Bot. 59, 3533-3542.
69. Shull, C.A., (1929) A spectrophotometric study of reflection of light from leaf surfaces. Bot. Gaz. 87, 583-607.
70. Sinclair, R., and, Thomas, D.A., (1970) Optical properties of leaves of some species in arid South Australia. Aust. J. Bot. 18, 261-273.
71. Sjodin, A., Street, N.R., Sandberg, G., Gustafsson, P., and, Jansson, S., (2009) The Populus Genome Integrative Explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytol. 182, 1013-1025.
72. Skaltsa, H., Verykokidou, E., Harvala, C., Karabourniotis, G., and, Manetas, Y., (1994) UV-B protective potential and flavonoids content of leaf hairs of Quercus ilex. Phytochemistry, 37, 987-990.
73. Smith, W.K., and, McClean, T.M., (1989) Adaptive relationship between leaf water repellency, stomatal distribution, and gas exchange. Am. J. Bot. 76, 465-469.
74. Smyth, G.K., (2005) Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor (, Gentleman, R.C., Carey, V.J., Dudoit, S., Irizarry, R., and, Huber, W., eds). New York: Springer, pp. 397-420.
75. Wilkins, O., Nahal, H., Foong, J., Provart, N.J., and, Campbell, M.M., (2009a) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol. 149, 981-993.
76. Wilkins, O., Waldron, L., Nahal, H., Provart, N.J., and, Campbell, M.M., (2009b) Genotype and time of day shape the Populus drought response. Plant J. 60, 703-715.
77. Woo, S.Y., (2010) Epidermal leaf characteristics and seasonal changes in net photosynthesis of five Populus. Afr. J. Biotechnol. 9, 1455-1458.
78. Wu, Z., Irizarry, R.A., Gentleman, R., Martinez-Murillo, F., and, Spencer, F., (2004) A Model-Based Background Adjustment for Oligonucleotide Expression Arrays. J. Am. Stat. Assoc. 99, 909-917.
79. Wu, Y., Machado, A.C., White, R.G., Llewellyn, D.J., and, Dennis, E.S., (2006) Expression profiling identifies genes expressed early during lint fibre initiation in cotton. Plant Cell Physiol. 47, 107-127.
80. Wuenscher, J.E., (1970) The effect of leaf hairs of Verbascum thapsus on leaf energy exchange. New Phytol. 69, 65-73.