Oilseed rape seeds with ablated defence cells of the glucosinolate- myrosinase system. Production and characteristics of double haploid MINELESS plants of Brassica napus L.

Journal of Experimental Botany

Volumn 62, Issue 14, 2011, Pages 4975-4993

  Ahuja, Ishita ^a   Borgen, Birgit Hafeld ^a,f   Hansen, Magnor ^b   Honne, Bjørn Ivar ^c   Müller, Caroline ^d   Rohloff, Jens ^a   Rossiter, John Trevor ^e   Bones, Atle Magnar ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c NORWEGIAN INSTITUTE OF BIOECONOMY RESEARCH   (Norway)

^d BIELEFELD UNIVERSITY   (Germany)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f SINTEF TECHNOLOGY AND SOCIETY   (Norway)

Author keywords

Brassica; double haploids; glucosinolates; homozygous; microspore culture; MINELESS; myrosin cell; myrosinase; oilseed rape; seed

Indexed keywords

GLUCOSINOLATE; GLYCOSIDASE; THIOGLUCOSIDASE; VEGETABLE PROTEIN;

ARTICLE; CYTOLOGY; ENZYMOLOGY; GENETICS; HAPLOIDY; METABOLISM; PLANT SEED; RAPESEED; TRANSGENIC PLANT;

BRASSICA NAPUS; GLUCOSINOLATES; GLYCOSIDE HYDROLASES; HAPLOIDY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEEDS;

BRASSICA; BRASSICA NAPUS; BRASSICACEAE;

EID: 80054119628     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err195     Document Type: Article

References (111)

1. Abdollahi M, Moieni A, Mousavi A, Salmanian A. 2010. High frequency production of rapeseed transgenic plants via combination of microprojectile bombardment and secondary embryogenesis of microspore-derived embryos. Molecular Biology Reports 38, 711-719.
2. Ahuja I, de Vos RCH, Bones AM, Hall RD. 2010a. Plant molecular stress responses face climate change. Trends in Plant Science 15, 664-674.
3. Ahuja I, Rohloff J, Bones AM. 2010b. Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review. Agronomy for Sustainable Development 30, 311-348.
4. Allen EJ, Morgan DG. 1972. A qualitative analysis of the effects of nitrogen on the growth, development and yield of oilseed rape. Journal of Agricultural Science 78, 315-324.
5. Andréasson D, Chakrabarty R, Bejai S, Zhang J, Rask L, Meijer J. 2009. Myrosinases from root and leaves of Arabidopsis thaliana have different catalytic properties. Phytochemistry 70, 1345-1354.
6. Andréasson E, Jørgensen LB, Hö glund AS, Rask L, Meijer J. 2001. Different myrosinase and idioblast distribution in Arabidopsis and Brassica napus. Plant Physiology 127, 1750-1763. (Pubitemid 34050038)
7. Bakr EM. 2005. A new software for measuring leaf area, and area damaged by Tetranychus urticae Koch. Journal of Applied Entomology 129, 173-175. (Pubitemid 40589041)
8. Bernardi R, Negri A, Ronchi S, Palmieri S. 2000. Isolation of the epithiospecifier protein from oil-rape (Brassica napus ssp oleifera) seed and its characterization. FEBS Letters 467, 296-298. (Pubitemid 30081753)
9. Björkman M, Klingen I, Birch ANE, et al. 2011. Phytochemicals of Brassicaceae in plant protection and human health-influences of climate, environment and agronomic practice. Phytochemistry 72, 538-556.
10. Bones A, Iversen TH. 1985. Myrosin cells and myrosinase. Israeli Journal of Botany 34, 351-375.
11. Bones A, Visvalingam S, Thangstad O. 1994. Sulphate can induce differential expression of thioglucoside glucohydrolases (myrosinases). Planta 193, 558-566. (Pubitemid 2078462)
12. Bones AM. 1990. Distribution of b-thioglucosidase activity in intact plants, cell and tissue cultures and regenerant plants of Brassica napus L. Journal of Experimental Botany 41, 737-744.
13. Bones AM, Rossiter JT. 1996. The myrosinase-glucosinolate system, its organisation and biochemistry. Physiologia Plantarum 97, 194-208. (Pubitemid 126616896)
14. Bones AM, Rossiter JT. 2006. The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67, 1053-1067. (Pubitemid 43833458)
15. Bones AM, Slupphaug G. 1989. Purification, characterization and partial amino acid sequencing of b-thioglucosidase from Brassica napus L. Journal of Plant Physiology 134, 722-729.
16. Bones AM, Thangstad OP, Haugen OA, Espevik T. 1991. Fate of myrosin cells: characterization of monoclonal-antibodies against myrosinase. Journal of Experimental Botany 42, 1541-1549.
17. Borgen BH, Thangstad OP, Ahuja I, Rossiter JT, Bones AM. 2010. Removing the mustard oil bomb from seeds: transgenic ablation of myrosin cells in oilseed rape (Brassica napus) produces MINELESS seeds. Journal of Experimental Botany 61, 1683-1697.
18. Brown PD, Morra MJ. 1995. Glucosinolate-containing plant tissues as bioherbicides. Journal of the Science of Food and Agriculture 43, 3070-3074.
19. Burow M, Bergner A, Gershenzon J, Wittstock U. 2007a. Glucosinolate hydrolysis in Lepidium sativum-identification of the thiocyanate-forming protein. Plant Molecular Biology 63, 49-61. (Pubitemid 44950231)
20. Burow M, Losansky A, Muller R, Plock A, Kliebenstein DJ, Wittstock U. 2009. The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis. Plant Physiology 149, 561-574.
21. Burow M, Markert J, Gershenzon J, Wittstock U. 2006. Comparative biochemical characterization of nitrile-forming proteins from plants and insects that alter myrosinase-catalysed hydrolysis of glucosinolates. FEBS Journal 273, 2432-2446. (Pubitemid 43736657)
22. Burow M, Rice M, Hause B, Gershenzon J, Wittstock U. 2007b. Cell-and tissue-specific localization and regulation of the epithiospecifier protein in Arabidopsis thaliana. Plant Molecular Biology 64, 173-185. (Pubitemid 46606929)
23. Cao MQ, Charlot F, Doŕe C. 1990. Embryogenesis and plant regeneration of sauerkraut cabbage (Brassica oleracea L. ssp. capitata) via in vitro isolated microspore culture. Comptes Rendus de l'Academie des Science Paris Serie III 310, 203-209.
24. Chay PM, Thurling N. 1989. Variation in pod length in spring rape (Brassica napus) and its effect on seed yield and yield components. Journal of Agricultural Science 113, 139-147.
25. Clossais-Besnard N, Larher F. 1991. Physiological role of glucosinolates in Brassica napus. Concentration and distribution pattern of glucosinolates among plant organs during a complete life cycle. Journal of the Science of Food and Agriculture 56, 25-38.
26. Custers JBM, Cordewener JHG, Nöllen Y, Dons HJM, Van Lookeren Campagne MM. 1994. Temperature controls both gametophytic and sporophytic development in microspore cultures of Brassica napus. Plant Cell Reports 13, 267-271. (Pubitemid 2040667)
27. Daun JK, McGregor DI. 1991. Glucosinolates in seeds and residues. London: Elsevier Applied Sciences.
28. Davis GRF, Campbell SJ, McGregor DI. 1981. Effect of commercial processing of canola and rapeseed on growth of larvae of the yellow mealworm, Tenebrio molitor L. Archives of Physiology and Biochemistry 89, 399-403.
29. Davis GRF, Campbell SJ, McGregor DI. 1983. Influence of canola hulls on gain in weight of larvae of the yellow mealworm, Tenebrio molitor L. Archives of Physiology and Biochemistry 91, 443-450.
30. Diepenbrock W. 2000. Yield analysis of winter oilseed rape (Brassica napus L.): a review. Field Crops Research 67, 35-49. (Pubitemid 30347702)
31. EC. 1990. Determination of the oilseed glucosinolate content by HPLC. Official Journal of the European Communities L170, 27-34.
32. Elfving S. 1980. Studies on the naturally occuring goitrogen 5-vinyl-2-thiooxazolidone. Metabolism and antithyroid effect in the rat. Annals of Clinical Research Suppl. 28, 1-47.
33. Eriksson S, André asson E, Ekbom B, Graner G, Pontoppidan B, Taipalensuu J, Zhang J, Rask L, Meijer J. 2002. Complex formation of myrosinase isoenzymes in oilseed rape seeds are dependent on the presence of myrosinase-binding proteins. Plant Physiology 129, 1592-1599. (Pubitemid 34923222)
34. Eriksson S, Ek B, Xue JP, Rask L, Meijer J. 2001. Identification and characterization of soluble and insoluble myrosinase isoenzymes in different organs of Sinapis alba. Physiologia Plantarum 111, 353-364.
35. Fageria NK. 1992. Biological yield, economic yield and harvest index. In: Fageria NK, ed. Maximizing cop yields. New York: Marcel Dekker, 10-13.
36. Fahey JW, Zalcmann AT, Talalay P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5-51. (Pubitemid 32063165)
37. Falk A, Taipalensuu J, Ek B, Lenman M, Rask L. 1995. Characterization of rapeseed myrosinase-binding protein. Planta 195, 387-395.
38. Fenwick GR, Heaney RK. 1983. Glucosinolates and their breakdown products in cruciferous crops, foods and feedingstuffs. Food Chemistry 11, 249-271.
39. Fletcher R, Coventry J, Kott LS. 1998. Double haploid technology for spring and winter Brassica napus. Guelph: OAC Publication.
40. Foo HL, Gronning LM, Goodenough L, Bones AM, Danielsen BE, Whiting DA, Rossiter JT. 2000. Purification and characterisation of epithiospecifier protein from Brassica napus: enzymic intramolecular sulphur addition within alkenyl thiohydroximates derived from alkenyl glucosinolate hydrolysis. FEBS Letters 468, 243-246. (Pubitemid 30110804)
41. Friedt W, Snowdon R. 2010. Oilseed rape. In: Vollmann J, Rajcan I, eds. Oil crops, Vol. 4. New York: Springer, 91-126.
42. Gabrielle B, Denoroy P, Gosse G, Justes E, Andersen M. 1998. A model of leaf area development and senescence of winter oilseed rape. Field Crops Research 57, 209-222. (Pubitemid 28259836)
43. Grubb CD, Abel S. 2006. Glucosinolate metabolism and its control. Trends in Plant Science 11, 89-100. (Pubitemid 43238420)
44. Guignard L. 1890. Sur la localization des principes qui fournissent les essences sulfurées des Crucifers. Comptes Rendus Hebdomadaires Seances de l'Academie des Sciences Serie III, 249-251.
45. Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57, 303-333. (Pubitemid 44061027)
46. Hansen M. 2003. Protocol for microspore culture in Brassica. Dordrecht: Kluwer Academic Publishers.
47. Hansen NJP, Andersen SB. 1996. In vitro chromosome doubling potential of colchicine, oryzalin, trifluralin and APM in Brassica napus microspore culture. Euphytica 88, 159-164. (Pubitemid 3040791)
48. Heaney RK, Spinks EA, Hanley AB, Fenwick GR. 1986. Technical bulletin: analysis of glucosinolates in rapeseed. Crowe, Norwich, UK: Agricultural and Food Research Council, Food Research Institute.
49. Himanen S, Nissinen A, Auriola S, Poppy G, Stewart C, Holopainen J, Nerg A-M. 2008. Constitutive and herbivore-inducible glucosinolate concentrations in oilseed rape (Brassica napus) leaves are not affected by Bt cry1Ac insertion but change under elevated atmospheric CO2 and O3. Planta 227, 427-437. (Pubitemid 351405271)
50. Höglund AS, Lenman M, Rask L. 1992. Myrosinase is localized to the interior of myrosin grains and is not associated to the surrounding tonoplast membrane. Plant Science, 85, 165-170.
51. Hopkins RJ, van Dam NM, van Loon JJA. 2009. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annual Review of Entomology 54, 57-83.
52. Husebye H, Chadchawan S, Winge P, Thangstad OP, Bones AM. 2002. Guard cell-and phloem idioblast-specific expression of thioglucoside glucohydrolase 1 (myrosinase) in Arabidopsis. Plant Physiology 128, 1180-1188. (Pubitemid 34305772)
53. Kasha KJ. 2005. Chromosome doubling and recovery of double haploids. Heidelberg: Springer Verlag.
54. Katiyar RK, Saran G, Giri G. 1986. Evaluation of Brassica carinata as a new oilseed crop in India. Experimental Agriculture 22, 67-70.
55. Kissen R, Bones AM. 2009. Nitrile-specifier proteins involved in glucosinolate hydrolysis in Arabidopsis thaliana. Journal of Biological Chemistry 284, 12057-12070.
56. Kissen R, Pope T, Grant M, Pickett J, Rossiter J, Powell G. 2009a. Modifying the alkylglucosinolate profile in Arabidopsis thaliana alters the tritrophic interaction with the herbivore Brevicoryne brassicae and parasitoid Diaeretiella rapae. Journal of Chemical Ecology 35, 958-969.
57. Kissen R, Rossiter J, Bones A. 2009b. The 'mustard oil bomb': not so easy to assemble?! Localization, expression and distribution of the components of the myrosinase enzyme system. Phytochemistry Reviews 8, 69-86.
58. Kliebenstein D, Pedersen D, Barker B, Mitchell-Olds T. 2002. Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161, 325-332. (Pubitemid 34564059)
59. Kucera V, Vyvadilovà M, Kĺma M. 2002. Utilization of doubled haploids in winter oilseed rape (Brassica napus L.) breeding. Czechoslovak Journal of Genetics and Plant Breeding 38, 50-54.
60. Lambrix V, Reichelt M, Mitchell-Olds T, Kliebenstein DJ, Gershenzon J. 2001. The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. The Plant Cell 13, 2793-2807. (Pubitemid 34088641)
61. Lankau RA, Strauss SY. 2007. Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317, 1561-1563. (Pubitemid 47417437)
62. Lenman M, Falk A, Rodin J, Hoglund AS, Ek B, Rask L. 1993. Differential expression of myrosinase gene families. Plant Physiology 103, 703-711. (Pubitemid 2023262)
63. Lenman M, Rodin J, Josefsson LG, Rask L. 1990. Immunological characterization of rapeseed myrosinase. European Journal of Biochemistry 194, 747-753.
64. Léon J, Becker HC. 1995. Rapeseed (Brassica napus L.) genetics. In: Diepenbrock W, Becker HC, eds. Physiological potentials for yield improvement of oil and protein crops. Advances in plant breeding, Vol. 17, 54-81.
65. Li Q, Eigenbrode SD, Stringam GR, Thiagarajah MR. 2000. Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. Journal of Chemical Ecology 26, 2401-2419.
66. Lichter R. 1982. Induction of haploid plants from isolated pollen of Brassica napus. Zeitschrift für Pflanzenphysiologie 105, 427-434.
67. Lüthy B, Matile P. 1984. The mustard oil bomb: rectified analysis of the subcellular organization of the myrosinase system. Biochemie und Physiologie der Pflanzen, 179, 5-12.
68. Mabon N, Wathelet JP, Marlier M. 1999. Analysis of 5-vinyl-1, 3-oxazolidine-2-thione in complex matrices at ppb level. Talanta 49, 199-206.
69. Major DJ, Charnetski WA. 1976. Distribution of 14C-labelled assimilates in rape plants. Crop Science 16, 530-532.
70. Malik MR, Wang F, Dirpaul JM, Zhou N, Hammerlindl J, Keller W, Abrams SR, Ferrie AMR, Krochko JE. 2008. Isolation of an embryogenic line from non-embryogenic Brassica napus cv. Westar through microspore embryogenesis. Journal of Experimental Botany 59, 2857-2873. (Pubitemid 351957507)
71. Matile P. 1980. The mustard oil bomb. Compartmentation of the myrosinase system. Biochemie und Physiologie der Pflanzen 175, 722-731.
72. Matthaus B, Luftmann H. 2000. Glucosinolates in members of the family Brassicaceae: separation and identification by LC/ESI-MS-MS. Journal of Agricultural and Food Chemistry 48, 2234-2239. (Pubitemid 30431218)
73. Matusheski NV, Swarup R, Juvik JA, Mithen R, Bennett M, Jeffery EH. 2006. Epithiospecifier protein from broccoli (Brassica oleracea L. ssp italica) inhibits formation of the anticancer agent sulforaphane. Journal of Agricultural and Food Chemistry 54, 2069-2076.
74. Mawson R, Heaney RK, Zdunczyk Z, Kozlowska H. 1993. Rapeseed meal-glucosinolates and their antinutritional effects 2. Flavor and palatability. Nahrung-Food 37, 336-344.
75. Mithen RF. 2001b. Glucosinolates and their degradation products. Advances in Botanical Research 35, 213-232.
76. Mollers C, Iqbal MCM, Robbelen G. 1994. Efficient production of double haploid Brassica napus plants by colchicine treatment of microspores. Euphytica 75, 95-104. (Pubitemid 2106005)
77. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473-497.
78. Pope T, Kissen R, Grant M, Pickett J, Rossiter J, Powell G. 2008. Comparative innate responses of the aphid parasitoid Diaeretiella rapae to alkenyl glucosinolate derived isothiocyanates, nitriles, and epithionitriles. Journal of Chemical Ecology 34, 1302-1310.
79. Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J. 2000. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Molecular Biology 42, 93-113. (Pubitemid 30097381)
80. Raybould AF, Moyes CL. 2001. The ecological genetics of aliphatic glucosinolates. Heredity 87, 383-391. (Pubitemid 34001950)
81. Rood SB, Major DJ. 1984. Influence of plant density, nitrogen, water supply and pod or leaf removal on growth of oilseed rape. Field Crops Research 8, 323-331.
82. Rosa EAS, Heaney RK, Fenwick GR, Portas CAM. 1997. Glucosinolates in crop plants. Horticultural Review 19, 99-215.
83. Sana M, Ali A, Asghar Malik M, Farrukh Saleem M, Rafik M. 2003. Comparative yield potential and oil contents of different canola cultivars (Brassica napus L.). Pakistan Journal of Agronomy 2, 1-7.
84. Sang JP, Minchinton IR, Johnstone PK, Truscott RJW. 1984. Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Canadian Journal of Plant Science 64, 77-93.
85. Shahidi F, Daun JK, De Clercq DR. 1997. Glucosinolates in Brassica oilseeds: processing effects and extraction. ACS Symposium Series. Washington, DC: American Chemical Society.
86. Shariatpanahi ME, Bal U, Heberle-Bors E, Touraev A. 2006. Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiologia Plantarum 127, 519-534. (Pubitemid 44065332)
87. Shi J, Li R, Qiu D, Jiang C, Long Y, Morgan C, Bancroft I, Zhao J, Meng J. 2009. Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182, 851-861.
88. Sidlakaus G, Bernotas S. 2003. Some factors affecting seed yield of spring oilseed rape (Brassica napus L.). Agronomy Research 1, 229-243.
89. Smolinska U, Morra MJ, Knudsen GR, Brown PD. 1997. Toxicity of glucosinolate degradation products from Brassica napus seed meal toward Aphanomyces euteiches f. sp. pisi. Phytopathology 87, 77-82. (Pubitemid 27132265)
90. Tayo TO, Morgan DG. 1979. Factors influencing flower and pod development in oilseed rape (Brassica napus L.). Journal of Agricultural Science 92, 363-373.
91. Thangstad OP, Evjen K, Bones A. 1991. Immunogold-EM localization of myrosinase in Brassicaceae. Protoplasma 161, 85-93.
92. Thangstad OP, Gilde B, Chadchawan S, Seem M, Husebye H, Bradley D, Bones AM. 2004. Cell specific, cross-species expression of myrosinases in Brassica napus, Arabidopsis thaliana and Nicotiana tabacum. Plant Molecular Biology 54, 597-611. (Pubitemid 39174911)
93. Thangstad OP, Iversen TH, Slupphaug G, Bones A. 1990. Immunocytochemical localization of myrosinase in Brassica napus L. Planta 180, 245-248.
94. Thurling N. 1974. Morphophysiological determinants of yield in rapeseed (Brassica campestris and Brassica napus). I Growth and morphological characters. Australian Journal of Agricultural Research 25, 697-710.
95. Thurling N. 1993. Physiological constraints and their genetic manipulation. Breeding oilseed Brassica. Springer Verlag: Narosa Publishing House, 44-66.
96. Touraev A, Vicente O, HeberleBors E. 1997. Initiation of microspore embryogenesis by stress. Trends in Plant Science 2, 297-302. (Pubitemid 27369346)
97. Travers-Martin N, Kuhlmann F, Mü ller C. 2008. Revised determination of free and complexed myrosinase activities in plant extracts. Plant Physiology and Biochemistry 46, 506-516.
98. Tripathi MK, Mishra AS. 2007. Glucosinolates in animal nutrition: a review. Animal Feed Science and Technology 132, 1-27. (Pubitemid 44712056)
99. Wallace SK, Eigenbrode SD. 2002. Changes in the glucosinolate-myrosinase defense system in Brassica juncea cotyledons during seedling development. Journal of Chemical Ecology 28, 243-256. (Pubitemid 34208177)
100. Weber S, Unker F, Friedt W. 2005. Improved doubled haploid production protocol for Brassica napus using microspore colchicine treatment in vitro and ploidy determination by flow cytometry. Plant Breeding 124, 511-513. (Pubitemid 41463379)
101. Winde I, Wittstock U. 2011. Insect herbivore counteradaptations to the plant glucosinolate-myrosinase system. Phytochemistry (in press).
102. Wittstock U, Burow M. 2010. Glucosinolate breakdown in Arabidopsis: mechanism, regulation and biological significance. The Arabidopsis Book 8, 1-14.
103. Yan XF, Chen SX. 2007. Regulation of plant glucosinolate metabolism. Planta 226, 1343-1352.
104. Young LW, Wilen RW, Bonham-Smith PC. 2004. High temperature stress of Brassica napus during flowering reduces micro-and megagametophyte fertility, induces fruit abortion, and disrupts seed production. Journal of Experimental Botany 55, 485-495. (Pubitemid 38204127)
105. Zabala MD, Grant M, Bones AM, Bennett R, Lim YS, Kissen R, Rossiter JT. 2005. Characterisation of recombinant epithiospecifier protein and its over-expression in Arabidopsis thaliana. Phytochemistry 66, 859-867. (Pubitemid 40545125)
106. Zhang L, Yang G, Liu P, Hong D, Li S, He Q. 2011. Genetic and correlation analysis of silique-traits in Brassica napus L. by quantitative trait locus mapping. Theoretical and Applied Genetics 122, 21-31.
107. Zhang W, Fu Q, Dai X, Bao M. 2008. The culture of isolated microspores of ornamental kale (Brassica oleracea var. acephala) and the importance of genotype to embryo regeneration. Scientia Horticulturae 117, 69-72.
108. Zhao J, Simmonds DH. 1995. Application of trifluralin to embryogenic microspore cultures to generate doubled haploid plants in Brassica napus. Physiologia Plantarum 95, 304-309. (Pubitemid 3004224)
109. Zhao J, Simmonds DH, Newcomb W. 1996. High frequency production of double haploid plants of Brassica napus cv. Topas derived from colchicine-induced microspore embryogenesis without heat shock. Plant Cell Reports 15, 668-671. (Pubitemid 26267393)
110. Zhao Z, Zhang W, Stanley BA, Assmann SM. 2008. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. The Plant Cell 20, 3210-3226.
111. Zhou WJ, Hagberg P, Tang GX. 2002. Increasing embryogenesis and doubling efficiency by immediate colchicine treatment of isolated microspores in spring Brassica napus. Euphytica 128, 27-34. (Pubitemid 35326005)