Hormone-response mutants of Arabidopsis thaliana (L.) Heynh. impaired in somatic embryogenesis

Plant Growth Regulation - Tập 49 - Trang 183-197 - 2006
Małgorzata D. Gaj1, Aneta Trojanowska1, Agnieszka Ujczak1, Martyna Mędrek1, Aleksandra Kozioł1, Beata Garbaciak1
1Department of Genetics, University of Silesia, Katowice, Poland

Tóm tắt

Plant hormones are considered to be the key factors involved in triggering in vitro induced plant morphogenesis, including somatic embryogenesis (SE). Mutants affected in SE and altered in hormonal response therefore provide valuable material for genetic research on in vitro induced plant embryogenesis. The capacity for SE was studied in 27 mutants with defects in response to different plant hormones: auxin, ABA, gibberellin and cytokinin, and evaluated in 2-week-old mutant and wild-type cultures in terms of their efficiency and productivity. SE was induced in vitro via a direct morphogenic pathway, through the culture of immature zygotic embryos on standard solid medium with 5 μM 2,4-D. The majority of the analyzed mutants displayed a significantly impaired capacity for SE; and those affected belonged to several different hormone-defective groups, including forms affected in auxin (axr4), gibberellin (ga) and ABA (abi, hyl1, cpb20, abh1) response. These mutants showed a significant decrease in embryogenic response as manifested by a low efficiency and/or productivity of SE. Additionally, SE efficiency was analyzed for axr4-1 mutant on media supplemented with different auxins while GA3 and inhibitors of gibberellins (uniconazol P and paclobutrazol), were applied for pkl1-1-mutant. The selected mutants provide a valuable research tool for studying the molecular mechanisms determining the induction of embryogenesis in cultures of somatic tissues. Their usefulness in further studies is discussed.

Tài liệu tham khảo

Bennet MJ, Marchant A, Green HG, May ST, Ward SP, Milner PA, Walker AR, Schultz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950 Besse I, Verdeil JL, Duval Y, Scotta B, Maldiney R, Miginiac E (1992) Oil palm (Elaeis guineesis Jacq.) clonal fidelity: endogenous cytokinins and indoleacetic acid in embryogenic callus cultures. J Exp Bot 43:983–989 Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren CMM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749 Braybrook SA, Stone SL, Park S, Bui Anhtthu Q, Brandon HL, Fischer R, Goldberg RB, John JH (2006) Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA 103:3468–3472 Brocard-Gifford IM, Lynch TJ, Finkelstein RR (2003) Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling. Plant Physiol 131:78–92 Charriere F, Hahne G (1998) Induction of embryogenesis versus caulogenesis on in vitro cultured sunflower (Helianthus annuus L.) immature zygotic embryos: role of plant growth regulators. Plant Sci 137:63–71 Charriere F, Sotta B, Migniac E, Hahne G (1999) Induction of adventitious shoots or somatic embryous on in vitro cultured zygotic embryos of Helianthus annuus: variation of endogenous hormone levels. Plant Physiol Biochem 37:751–757 Cheng JT, Chang WCh (2003) Effects of GA3, ancymidol, cycocel and paclobutrazol on direct somatic embryogenesis of Oncidium in vitro. Plant Cell Tissue Org Cult 72:105–108 Choi YE, Kim HS, Soh WY, Yang DC (1997) Development and structural aspects of somatic embryos formed on medium containing 2,3,5-triiodobenzoic acid. Plant Cell Rep 16:738–744 Chung HH, Chen JT, Chang WCh (2005) Cytokinins induced direct somatic embryogenesis of Dendrobium chiengmai pink and subsequent plant regeneration. In Vitro Cell Develop Biol Plant 41:765–769 Curaba J, Moritz R, Blervaque R, Parcy F, Raz V, Herzog M, Vachon G (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin biosynthesis, is regulated during embryogenesis by LEAFY COTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol 136:3660–3669 Delbbare A, Muller P, Imhoff V, Gueren J (1996) Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlrophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:532–541 Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M, Marchant A, Mills S, Sandberg G, Bennett MJ, Estelle M (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220 Dudits D, Gyorgyey J, Bogre L, Bako L (1995) Molecular biology of somatic embrygenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer Academic Publishers, Dordrecht, pp 267–308 Etienne H, Scotta B, Montoro P, Miginiac E, Carron MP (1993) Relation between exogenous growth regulators and endogenous indole-3-acetic acid and abscisic acid in the expression of somatic embryogenesis in Hevea brasilliensis (Müll Arg.). Plant Sci 88:91–96 Ezhova TA (2003) Genetic control of totipotency of plant cells in an in vitro culture. Rus J Devel Biol 34:245–252 Feher A (2005) Why somatic cells start to form embryos?. Plant Cell Monogr 2:1–17 Feher A, Pasternak TP, Dudits D (2003) Transient of somatic plant cells to an embryogenic state. Plant Cell Tissue Org Cult 74:201–228 Fernando SC, Gamage CKA (2000) Abscisic acid induced somatic embryogenesis in immature embryo explant of coconut (Cocos nucifere L.). Plant Sci 151:193–198 Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45 Fiore CM, Trabace T, Sunseri F (1997) High frequency of plant regeneration in sunflower from cotyledons via somatic embryogenesis. Plant Cell Rep 16:295–298 Gaj MD (2001) Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana (L.) Heynh. plants. Plant Cell Tissue Org Cult 64:39–46 Gaj MD (2004) Factors influencing somatic embryogenesis induction and plant regeneration with particular reference to Arabidopsis thaliana (L.) Heynh. Plant Growth Regul 43:27–47 Gaj MD, Zhang S, Harada J, Lemaux PG (2005) LEAFY COTYLEDON genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988 Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirement of suspension cultures of soybean root cells. Exp Cell Res 50:151–158 Gazzarrini S, McCourt P (2003) Cross-talk in plant hormone signaling: what Arabidopsis mutants are telling us. Ann Bot 91:605–612 Grossmann K, Hansen H (2001) Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiol Plant 113:9–14 Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsisdouble stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101:1093–1098 Harada JJ (1999) Signalling in plant embryogenesis. Curr Opin Plant Biol 2:23–27 Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant Physiol 133:653–663 Henderson JT, Li HCH, Rider SD, Mordhorst AP, Romero-Severson J, Cheng JCH, Robey J, Sung ZR, de Vries SC, Ogas J (2004) PICKLE acts through the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134:995–1005 Hobbie L, Estelle MA (1995) The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. Plant J 7:211–220 Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI (2002) Localization, ion channel regulation, and genetic interactions during abscisic acid signaling of nuclear mRNA cap binding protein, ABH1. Plant Physiol 130:1276–1287 Ivanova A, Velcheva M, Denchev P, Atanassow A, van Onckelen H (1994) Endogenous hormone levels during direct somatic embryogenesis in Medicago falcata. Physiol Plant 92:85–89 Jenik PD, Barton MK (2005) Surge and destroy: the role of auxin in plant embryogenesis. Development 132:3577–3585 Jiménez VM (2005) Involvement of plant hormones and plant growth regulators on in vitro somatic embryogenesis. Plant Growth Reg 47:91–110 Jiménez VM, Bangerth F (2001a) Endogenous hormone levels in explants and in embryogenic and non-embryogenic cultures of carrot. Physiol Plant 111:389–395 Jiménez VM, Bangerth F (2001b) Hormonal status of maize initial explants and of the embryogenic and non-embryogenic callus cultures derived from them as related to morphogenesis in vitro. Plant Sci 160:247–257 Kagaya Y, Okuda R, Ban A, Toyoshim R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005a) Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46:300–311 Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005b) LEAFY COTYLEDON 1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46:399–406 Kikuchi A, Sanuki N, Higashi K, Koshiba T, Kamada H (2005) Abscisic acid and stress treatment are essential for the acquisition of embryonic competence by carrot somatic cells. Planta 222:977–988 Leon P, Sheen J (2003) Sugar and hormone connections. Trends in Plant Sci 8:110–116 Luo Y, Koop HS (1997) Somatic embryogenesis in cultured immature zygotic embryos and leaf protoplasts of Arabidopsis thaliana ecotypes. Planta 202:387–396 Mendoza MS, Dubreucq B, Miquel M, Cabocla M, Lepiniec L (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett 579:4666–4670 Michalczuk L, Druart P (1999) Indole-3-acetic acid metabolism in hormone autotrophic, embryogenic calls of Inmil cherry rootstock (Prunus incise × serrula ‘GM 9) and in hormone-dependent, nonembryogenic calli of Prunus incise × serula and Prunus domestica. Physiol Plant 107:426–432 Michalczuk L, Cooke TJ, Cohen JD (1992) Auxin level at different stages of carrot somatic embryogenesis. Phytochemistry 31:1097–1103 Mitsuhashi W, Toyomasu T, Masui H, Katho T, Nakaminami K, Kashiwagi Y, Akutsu M, Kenmoku H, Sassa T, Yamaguchi S, Kamiya Y, Kamada H (2003) Gibberellin is essentially required for carrot (Daucus carota L.) somatic embryogenesis: dynamics regulation of gibberellin 3-oxidase gene expressions. Biosci Biotechnol Biochem 67:2438–2447 Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, van Went J, Koornneef M, deVries SC (1998) Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutation in genes repressing meristematic cell divisions. Genetics 149:549–563 Nakagawa H, Saijyo T, Yamauchi N, Shigyo M, Kako S, Ito A (2001) Effects of sugars and abscisic acid on somatic embryogenesis from melon (Cucumis melo L.) expanded cotyledon. Sci Hort 90:85–92 Niyogi KK, Grossman AR, Bjorkman O (1998) Arabidopsis mutants define a central role for the xanthophylls cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–1134 Ogas J, Cheng ChJ, Sung ZR, Somerville Ch (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–93 Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844 Ogata Y, Iizuka M, Nakayama D, Ikeda M, Kamada H, Koshiba T (2005) Possible involvement of abscisic acid in the induction of secondary somatic embryogenesis on seed-coat-derived carrot somatic embryos. Planta 221:417–423 Papp I, Mur LA, Dalmadi A, Dulai S, Koncz C (2004) Mutation in the Cap Binding Protein 20 gene confers drought tolerance to Arabidopsis. Plant Mol Biol 55:79–86 Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, van Onckelen HA, Dudits D, Feher A (2002) The role of auxins, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819 Pintos B, Martin JP, Centeno ML, Villalobos N, Guerra H, Martin L (2002) Endogenous cytokinin levels in embryogenic and non-embryogenic calli of Medicago arborea L. Plant Sci 163:955–960 Pullman GS, Mein J, Johnson S, Zhang Y (2005) Gibberellin inhibitors improve embryogenic tissue initiation in conifers. Plant Cell Rep 23:596–605 Rock CD, Sun X (2005) Crosstalk between ABA and auxin signaling pathways in roots of Arabidopsis thaliana (L.) Heynh. Planta 222:98–106 Ruduś I, Kępczyńska E, Kępczyński J (2002) Regulation of Medicago sativa L. somatic embryogenesis by gibberellins. Plant Growth Regul 36:91–95 Sagare AP, Lee YL, Lin TC, Chen CC, Tsay HS (2000) Cytokinin-induced somatic embryogenesis and plant regeneration in Corydalis yanhusuo (Fumariaceae) – a medicinal plant. Plant Sci 160:139–147 Schwartz SH, Leon-Kloosterziel KM, Koornneef M, Zeevaart JA (1997) Biochemical characterisation of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol 114:161–166 Senger S, Mock HP, Conrad U, Manteuffel R (2001) Immunomodulation of ABA function affects early events in somatic embryo development. Plant Cell Rep 20:112–120 Söderman EM, Brocard IM, Lynch TJ, Finkelstein RR (2000) Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol 124:752–765 Thomas C, Bronner R, Prinsen JME, van Onckelen H, Hahne G (2002) Immuno-cytochemical localization of indole-3-acetic acid during induction of somatic embryogenesis in cultured sunflower embryos. Planta 215:577–583 Tokuji Y, Kuriyama K (2003) Involvement of gibberellin and cytokinin in the formation of embryogenic cell clumps in carrot (Daucus carota). J Plant Physiol 160:133–141 von Recklinghausen IR, Iwanowska A, Kieft H, Mordhorst AP, Schel JHN, von Lammeren AAM (2000) Structure and development of somatic embryos formed in Arabidopsis pt mutant callus cultures derived from seedlings. Protoplasma 211:217–224 Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding and enzyme involved in gibberellin metabolism. Plant Cell 16:1206–1219 Wenck AR, Conger BV, Trigiano RN, Sams CE (1988) Inhibition of somatic embryogenesis in orchardgrass by endogenous cytokinins. Plant Physiol 88:990–992 Wu IF, Chen JT, Chang WC (2004) Effects of auxins and cytokinins on embryo formation from callus of Oncidium ‘Gower Ramsey’. Plant Cell Tiss Org Cult 77:107–109 Wu Y, Haberland G, Zhou C, Koop HU (1992) Somatic embryogenesis, formation of morphogenic callus and normal development in zygotic embryos of Arabidopsis thaliana in vitro. Protoplasma 169:89–96 Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359