Brassica villosa, a system for studying non-glandular trichomes and genes in the Brassicas

Plant Molecular Biology

Volumn 85, Issue 4, 2014, Pages 519-539

  Nayidu, Naghabushana K ^a,b   Tan, Yifang ^c   Taheri, Ali ^a   Li, Xiang ^d   Bjorndahl, Trent C ^e   Nowak, Jacek ^c   Wishart, David S ^e   Hegedus, Dwayne ^a   Gruber, Margaret Y ^a  

^a SASKATOON RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d JILIN UNIVERSITY   (China)

^e UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Brassica napus; Brassica villosa; Global gene expression; Metals; Secondary metabolites; Trichome preparations

Indexed keywords

ARABIDOPSIS; BRASSICA; BRASSICA NAPUS; BRASSICA VILLOSA; HEXAPODA;

METAL; VEGETABLE PROTEIN;

ARTICLE; BRASSICA; GENE EXPRESSION REGULATION; GENETICS; HISTOLOGY; METABOLISM; PHYSIOLOGY; PLANT LEAF; PROTEIN MICROARRAY; SEEDLING; TRICHOME;

BRASSICA; GENE EXPRESSION REGULATION, PLANT; METALS; PLANT LEAVES; PLANT PROTEINS; PROTEIN ARRAY ANALYSIS; SEEDLING; TRICHOMES;

EID: 84902330083     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-014-0201-1     Document Type: Article

References (104)

1. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R (2002) Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56: 2206-2213.
2. Agren J, Schemske DW (1992) Artificial selection on trichome number in Brassica rapa. Theor Appl Genet 83: 673-678.
3. Agren J, Schemske DW (1993) The cost of defense against herbivores: an experimental study of trichome production in Brassica rapa. Am Nat 141: 338-350.
4. Agren J, Schemske DW (1994) Evolution of trichome number in a naturalized population of Brassica rapa. Am Nat 143: 1-13.
5. Aziz N, Paiva NL, May GD, Dixon RA (2005) Transcriptome analysis of alfalfa glandular trichomes. Planta 221: 28-38.
6. Balkunde R, Pesch M, Hülskamp M (2010) Chapter ten trichome patterning in Arabidopsis thaliana: from genetic to molecular models. Curr Top Dev Biol 91: 299-321.
7. Bax AD, Davis DG (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J Magn Reson 65: 355-360.
8. Bax A, Subramanian S (1986) A proton-detected heteronuclear chemical-shift correlation experiment with improved resolution and sensitivity. J Magn Reson 86: 346-357.
9. Bax A, Summers MF (1986) Proton and carbon-13 assignments from sensitivity-enhanced detection of heteronuclear multiple-bond connectivity by 2D multiple quantum NMR. J Am Chem Soc 108: 2093-2094.
10. Bax AD, Griffey RH, Hawkins BL (1983) Correlation of proton and nitrogen-15 chemical shifts by multiple quantum NMR. J Magn Reson 1969(55): 301-315.
11. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodological) 57: 289-300.
12. Bhalla PL, Singh MB (2008) Agrobacterium-mediated transformation of Brassica napus and Brassica oleracea. Nat Protoc 3: 181-189.
13. Bigger CB, Brasky KM, Lanford RE (2001) DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J Virol 75: 7059-7066.
14. Bouchereau A, Hamelin J, Lamour I, Renard M, Larher F (1991) Distribution of sinapine and related compounds in seeds of Brassica and allied genera. Phytochemistry 30: 1873-1881.
15. Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M, Wester K, Balkunde R, Timmer J, Fleck C, Hülskamp M (2008) Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol 6: e141.
16. Branca F, Bas N, Artemyeva A, De Haro A, Maggioni L (2012) In progress activities of the Brassica Working Group of the European Cooperative Programme for Plant Genetic Resources (ECPGR). Joint 6th ISHS international symposium on Brassicas and 18th crucifer genetics workshop. Catania, Italy, pp 12-16.
17. Braunschweiler L, Ernst RR (1983) Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J Magn Reson (1969) 53: 521-528.
18. Broadhurst CL, Chaney RL, Angle JS, Erbe EF, Maugel TK (2004) Nickel localization and response to increasing Ni soil levels in leaves of the Ni hyperaccumulator Alyssum murale. Plant Soil 265: 225-242.
19. Chismar J, Mondala T, Fox H, Roberts E, Langford D, Masliah E, Salomon D, Head S (2002) Analysis of result variability from high-density oligonucleotide arrays comparing same-species and cross-species hybridizations. Biotechniques 33: 516-518, 520, 522 passim.
20. Choi YE, Harada E (2005) Roles of calcium and cadmium on Cd-containing intra-and extracellular formation of Ca crystals in tobacco. J Plant Biol 48: 113-119.
21. Choi YE, Harada E, Wada M, Tsuboi H, Morita Y, Kusano T, Sano H (2001) Detoxification of cadmium in tobacco plants: formation and active excretion of crystals containing cadmium and calcium through trichomes. Planta 213: 45-50.
22. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
23. 2+ by trichomes. Planta 214: 158-162.
24. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax AD (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
25. Deng S, Yun G, Zhang Q, Xu HL, Cai Q (2004) Effect of false flax (Camelina sativa) on larval feeding and adult behavioral response of the diamondback moth (Plutella xylostella). Acta Entomol Sin 4: 010.
26. Diez-Tascón C, Keane OM, Wilson T, Zadissa A, Hyndman DL, Baird DB, McEwan JC, Crawford AM (2005) Microarray analysis of selection lines from outbred populations to identify genes involved with nematode parasite resistance in sheep. Physiol Genomics 21: 59-69.
27. Digiuni S, Schellmann S, Geier F, Greese B, Pesch M, Wester K, Dartan B, Mach V, Srinivas BP, Timmer J (2008) A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves. Mol Syst Biol 4: 217-225.
28. Donaldson L, Vuocolo T, Gray C, Strandberg Y, Reverter A, McWilliam S, Wang Y, Byrne K, Tellam R (2005) Construction and validation of a bovine innate immune microarray. BMC Genom 6: 135.
29. Esch JJ, Chen MA, Hillestad M, Marks MD (2004) Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J 40: 860-869.
30. Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Biol 52: 29-66.
31. Gaeta RT, Yoo S-Y, Pires J, Doerge R, Chen ZJ, Osborn TC (2009) Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS ONE 4: e4760.
32. Gao Y, Gong X, Cao W, Zhao J, Fu L, Wang X, Schumaker KS, Guo Y (2008) SAD2 in Arabidopsis functions in trichome initiation through mediating GL3 function and regulating GL1, TTG1 and GL2 expression. J Integr Plant Biol 50: 906-917.
33. Gilad Y, Borevitz J (2006) Using DNA microarrays to study natural variation. Curr Opin Genet Dev 16: 553-558.
34. Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J (2000) Microarray analysis of developing Arabidopsis seeds. Plant Physiol 124: 1570-1581.
35. Gomez Campo C, Tortosa ME (1974) The taxonomic and evolutionary significance of some juvenile characters in the Brassiceae. Bot J Linn Soc 69: 105-124.
36. Gomez-Campo C, Tortosa ME, Tewari I, Tewari JP (1999) Epicuticular wax columns in cultivated brassica species and in their close wild relatives. Ann Bot 83: 515-519.
37. Gresham D, Dunham MJ, Botstein D (2008) Comparing whole genomes using DNA microarrays. Nat Rev Genet 9: 291-302.
38. Gutiérrez-Alcalá G, Gotor C, Meyer AJ, Fricker M, Vega JM, Romero LC (2000) Glutathione biosynthesis in Arabidopsis trichome cells. Proc Natl Acad Sci 97: 11108-11113.
39. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57: 303-333.
40. Henderson FG, Chen KK (1950) The pharmacology of lunarine, the alkaloid of Lunaria biennis. J Am Pharm Assoc 39: 516-519.
41. Horiguchi G, Nakayama H, Ishikawa N, Kubo M, Demura T, Fukuda H, Tsukaya H (2011) ANGUSTIFOLIA3 plays roles in adaxial/abaxial patterning and growth in leaf morphogenesis. Plant Cell Physiol 52: 112-124.
42. Horvath DP, Schaffer R, West M, Wisman E (2003) Arabidopsis microarrays identify conserved and differentially expressed genes involved in shoot growth and development from distantly related plant species. Plant J 34: 125-134.
43. Huang J, Bhinu VS, Li X, Bashi ZD, Zhou R, Hannoufa A (2009) Pleiotropic changes in Arabidopsis f5h and sct mutants revealed by large-scale gene expression and metabolite analysis. Planta 230: 1057-1069.
44. Huff JL, Hansen LM, Solnick JV (2004) Gastric transcription profile of Helicobacter pylori infection in the rhesus macaque. Infect Immun 72: 5216-5226.
45. Isaure MP, Fayard B, Sarret G, Pairis S, Bourguignon J (2006) Localization and chemical forms of cadmium in plant samples by combining analytical electron microscopy and X-ray spectromicroscopy. Spectrochim Acta, Part B 61: 1242-1252.
46. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59: 365-386.
47. Jeener J, Meier BH, Bachmann P, Ernst RR (1979) Investigation of exchange processes by two dimensional NMR spectroscopy. J Chem Phys 71: 4546.
48. Johnson BA, Blevins RA (1994) NMR view: a computer program for the visualization and analysis of NMR data. J Biomol NMR 4: 603-614.
49. Kang BH, Busse JS, Bednarek SY (2003) Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. The Plant Cell Online 15: 899-913.
50. Kift NB, Ellis PR, Tatchell GM, Pink DAC (2000) The influence of genetic background on resistance to the cabbage aphid (Brevicoryne brassicae) in kale (Brassica oleracea var. acephala). Ann Appl Biol 136: 189-195.
51. Kim JS, Jung HJ, Lee HJ, Kim K, Goh CH, Woo Y, Oh SH, Han YS, Kang H (2008) Glycine rich RNA binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J 55: 455-466.
52. Kirik V, Simon M, Huelskamp M, Schiefelbein J (2004) The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268: 506-513.
53. Koona P, Jackai LEN (2004) The potential of pod-shaving in studies of the role of trichomes in Vigna resistance to the pod-bug Clavigralla tomentosicollis Stål (Hemiptera: Coreidae). Int J Trop Insect Sci 24: 298-303.
54. Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212: 75-84.
55. Küpper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52: 2291-2300.
56. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, Sano R, Nagasaka R, Tominaga R, Koshino-Kimura Y, Kato T (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132: 5387-5398.
57. Lange BM, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, Croteau R (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc Natl Acad Sci 97: 2934-2939.
58. Lee HS, Wang J, Tian L, Jiang H, Black MA, Madlung A, Watson B, Lukens L, Pires JC, Wang JJ (2004) Sensitivity of 70-mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotechnol J 2: 45-57.
59. Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48: 3-15.
60. Liu R, Zhao J, Xiao Y, Meng J (2005) Identification of prior candidate genes for Sclerotinia local resistance in Brassica napus using Arabidopsis cDNA microarray and Brassica-Arabidopsis comparative mapping. Sci China, Ser C Life Sci 48: 460-470.
61. Mathur J (2006) Trichome cell morphogenesis in Arabidopsis: a continuum of cellular decisions. This review is one of a selection of papers published in the Special Issue on Plant Cell Biology. Botany 84: 604-612.
62. McNear DH Jr, Peltier E, Everhart J, Chaney RL, Sutton S, Newville M, Rivers M, Sparks DL (2005) Application of quantitative fluorescence and absorption-edge computed microtomography to image metal compartmentalization in Alyssum murale. Environ Sci Technol 39: 2210-2218.
63. Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56: 2885-2895.
64. Mozes-Koch R, Gover O, Tanne E, Peretz Y, Maori E, Chernin L, Sela I (2012) Expression of an entire bacterial operon in plants. Plant Physiol 158: 1883-1892.
65. Nayidu NK, Kagale S, Taheri A, Withana-Gamage TS, Parkin IA, Sharpe AG, Gruber MY (2014) Comparison of five major trichome regulatory genes in Brassica villosa with Orthologues within the Brassicaceae. PLoS ONE 9: e95877.
66. Ojangu EL, Tanner K, Pata P, Järve K, Holweg CL, Truve E, Paves H (2012) Myosins XI-K, XI-1, and XI-2 are required for development of pavement cells, trichomes, and stigmatic papillae in Arabidopsis. BMC Plant Biol 12: 81.
67. Oshlack A, Chabot AE, Smyth GK, Gilad Y (2007) Using DNA microarrays to study gene expression in closely related species. Bioinformatics 23: 1235-1242.
68. Otting G, Wüthrich K (1989) Extended heteronuclear editing of 2D 1H NMR spectra of isotope-labeled proteins, using the X(w1, w2)-double-half-filter. J Magn Reson 85: 586-594.
69. Palaniswamy P, Bodnaryk RP (1994) A wild Brassica from Sicily provides trichome-based resistance against flea beetles, Phyllotreta cruciferae (Goeze) (Coleoptera: Chrysomelidae). Can Entomol 126: 1119-1130.
70. Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H (1987) The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J 6: 3553.
71. Pesch M, Hülskamp M (2004) Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Curr Opin Genet Dev 14: 422-427.
72. Pesch M, Hülskamp M (2009) One, two, three... models for trichome patterning in Arabidopsis? Curr Opin Plant Biol 12: 587-592.
73. Piantini U, Sorensen OW, Ernst RR (1982) Multiple quantum filters for elucidating NMR coupling networks. J Am Chem Soc 104: 6800-6801.
74. Ramsey AD, Ellis PR (1994) Resistance in wild Brassicas to the Cabbage white fly, Aleyrodes proletella ISHS Brassica symposium-IX crucifer genetics workshop 407, pp 507-514.
75. Sallaud C, Giacalone C, Töpfer R, Goepfert S, Bakaher N, Rösti S, Tissier A (2012) Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes. Plant J 72: 1-17.
76. Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109: 1427-1433.
77. Schellmann S, Hulskamp M (2005) Epidermal differentiation: trichomes in Arabidopsis as a model system. Int J Dev Biol 49: 579.
78. Scialabba A, Di Liberto C, Dell'Aquila A (1999) Salt-treatment integrated germination test in the evaluation of Brassica villosa subsp. Drepanensis seed quality. Seed Sci Technol 27: 865-870.
79. Shi C, Thümmler F, Melchinger AE, Wenzel G, Lübberstedt T (2006) Comparison of transcript profiles between near-isogenic maize lines in association with SCMV resistance based on unigene-microarrays. Plant Sci 170: 159-169.
80. Singh SP, Sachan GC (1997) Effect of different temperatures and host plants on the developmental behaviour of mustard sawfly, Athalia proxima. Indian J Entomol 59: 34-40.
81. Smyth G (2005) Limma: linear models for microarray data. Bioinform Comput Biol Solut R Bioconduct 2005: 397-420.
82. Snogerup S, Gustafsson M, Von Bothmer R (1990) Brassica sect. Brassica (Brassicaceae) I. Taxonomy and variation. Willdenowia 19: 271-365.
83. Taylor DC, Falk KC, Palmer CD, Hammerlindl J, Babic V, Mietkiewska E, Jadhav A, Marillia EF, Francis T, Hoffman T (2010) Brassica carinata-a new molecular farming platform for delivering bio-industrial oil feedstocks: case studies of genetic modifications to improve very long-chain fatty acid and oil content in seeds. Biofuels, Bioprod Biorefin 4: 538-561.
84. Teoh KH, Polichuk DR, Reed DW, Nowak G, Covello PS (2006) Artemisia annua L. (Asteraceae) trichome-specific cDNAs reveal CYP71AV1, a cytochrome P450 with a key role in the biosynthesis of the antimalarial sesquiterpene lactone artemisinin. FEBS Lett 580: 1411-1416.
85. Tominaga R, Iwata M, Sano R, Inoue K, Okada K, Wada T (2008) Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135: 1335-1345.
86. Traw BM, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131: 526-532.
87. Trick M, Cheung F, Drou N, Fraser F, Lobenhofer EK, Hurban P, Magusin A, Town CD, Bancroft I (2009) A newly-developed community microarray resource for transcriptome profiling in Brassica species enables the confirmation of Brassica-specific expressed sequences. BMC Plant Biol 9: 50.
88. U (1935) N: Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7: 389-452.
89. Vahey MT, Nau ME, Taubman M, Yalley-Ogunro J, Silvera P, Lewis MG (2003) Patterns of gene expression in peripheral blood mononuclear cells of rhesus macaques infected with SIVmac251 and exhibiting differential rates of disease progression. AIDS Res Hum Retrovir 19: 369-387.
90. van Ooik T, Pausio S, Rantala MJ (2008) Direct effects of heavy metal pollution on the immune function of a geometrid moth, Epirrita autumnata. Chemosphere 71: 1840-1844.
91. Velasco L, Goffman FD, Becker HC (1998) Variability for the fatty acid composition of the seed oil in a germplasm collection of the genus Brassica. Genet Resour Crop Evol 45: 371-382.
92. Velasco P, Soengas P, Vilar M, Cartea ME, del Rio M (2008) Comparison of glucosinolate profiles in leaf and seed tissues of different Brassica napus crops. J Am Soc Hortic Sci 133: 551-558.
93. Wagner G, Wüthrich K (1982) Amide proton exchange and surface conformation of the basic pancreatic trypsin inhibitor in solution: studies with two-dimensional nuclear magnetic resonance. J Mol Biol 160: 343-361.
94. Wang S, Kwak S-H, Zeng Q, Ellis BE, Chen X-Y, Schiefelbein J, Chen J-G (2007) TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873-3882.
95. Wang G, Tian L, Aziz N, Broun P, Dai X, He J, King A, Zhao PX, Dixon RA (2008) Terpene biosynthesis in glandular trichomes of hop. Plant Physiol 148: 1254-1266.
96. Warwick S (2011) Brassicaceae in agriculture. In: Schmidt R, Bancroft I (eds) Genetics and genomics of the Brassicaceae, plant genetics and genomics crops and models 9. Springer Science + Business Media, LLC. doi: 10. 1007/978-1-4419-7118-0_2.
97. Wester K, Digiuni S, Geier F, Timmer J, Fleck C, Hülskamp M (2009) Functional diversity of R3 single-repeat genes in trichome development. Development 136: 1487-1496.
98. Wienkoop S, Zoeller D, Ebert B, Simon-Rosin U, Fisahn J, Glinski M, Weckwerth W (2004) Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification. Phytochemistry 65: 1641-1649.
99. Wilson IW, Kennedy GC, Peacock JW, Dennis ES (2005) Microarray analysis reveals vegetative molecular phenotypes of Arabidopsis flowering-time mutants. Plant Cell Physiol 46: 1190-1201.
100. Wink M (1992) Insect plant interactions. In: Bernays EA (ed) Insect plant interactions. CRC Press, Boca Raton.
101. Wink M (1993) The alkaloids. In: Cordell G (ed) The alkaloids. Academic Press, New York.
102. Zhang X, Oppenheimer DG (2004) A simple and efficient method for isolating trichomes for downstream analyses. Plant Cell Physiol 45: 221-224.
103. Zhu T, Chang H-S, Schmeits J, Gil P, Shi L, Budworth P, Zou G, Chen X, Wang X (2001) Gene expression microarrays: improvements and applications towards agricultural gene discovery. J Assoc Lab Autom 6: 95-98.
104. Zimeri AM, Dhankher OP, McCaig B, Meagher RB (2005) The plant MT1 metallothioneins are stabilized by binding cadmiums and are required for cadmium tolerance and accumulation. Plant Mol Biol 58: 839-855.