Abstract
Main conclusion
Microscopic techniques remain an integral tool which has allowed for the better understanding and manipulation of in vitro plant culture systems. The recent advancements will inevitably help to unlock the long-standing mysteries of fundamental biological mechanisms of plant cells.
Beyond the classical applications in micropropagation aimed at the conservation of endangered and elite commercial genotypes, plant cell, tissue and organ cultures have become a platform for elucidating a myriad of fundamental physiological and developmental processes. In conjunction with microscopic techniques, in vitro culture technology has been at the centre of important breakthroughs in plant growth and development. Applications of microscopy and plant tissue culture have included elucidation of growth and development processes, detection of in vitro-induced physiological disorders as well as subcellular localization using fluorescent protein probes. Light and electron microscopy have been widely used in confirming the bipolarity of somatic embryos during somatic embryogenesis. The technique highlights basic anatomical, structural and histological evidence for in vitro-induced physiological disorders during plant growth and development. In this review, we discuss some significant biological insights in plant growth and development, breakthroughs and limitations of various microscopic applications and the exciting possibilities offered by emergent in vivo live imaging and fluorescent protein engineering technologies.
Similar content being viewed by others
References
Ascough GD, Novák O, Pěnčík A, Rolčík J, Strnad M, Erwin JE, Van Staden J (2009) Hormonal and cell division analyses in Watsonia lepida seedlings. J Plant Physiol 166:1497–1507
Bairu MW, Kane ME (2011) Physiological and developmental problems encountered by in vitro cultured plants. Plant Growth Regul 63:101–103
Bairu MW, Stirk WA, Van Staden J (2009) Factors contributing to in vitro shoot-tip necrosis and their physiological interactions. Plant Cell Tissue Organ Cult 98:239–248
Bairu MW, Aremu AO, Van Staden J (2011) Somaclonal variation in plants: causes and detection methods. Plant Growth Regul 63:147–173
Bird DA, Buruiana MM, Zhou Y, Fowke LC, Wang H (2007) Arabidopsis cyclin-dependent kinase inhibitors are nuclear-localized and show different localization patterns within the nucleoplasm. Plant Cell Rep 26:861–872
Blazquez S, Olmos E, Hernández JA, Fernández-García N, Fernández JA, Piqueras A (2009) Somatic embryogenesis in saffron (Crocus sativus L.). Histological differentiation and implication of some components of the antioxidant enzymatic system. Plant Cell Tissue Organ Cult 97:49–57
Boevink P, Oparka K, Cruz SS, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447
Bouchabké-Coussa O, Obellianne M, Linderme D, Montes E, Maia-Grondard A, Vilaine F, Pannetier C (2013) Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Rep 32:675–686
Canhoto JM, Mesquita JF, Cruz GS (1996) Ultrastructural changes in cotyledons of pineapple guava (Myrtaceae) during somatic embryogenesis. Ann Bot 78:513–521
Canhoto JM, Rama SC, Cruz GS (2006) Somatic embryogenesis and plant regeneration in carob (Ceratonia siliqua L.). In Vitro Cell Dev Biol-Plant 42:514–519
Canter PH, Thomas H, Ernst E (2005) Bringing medicinal plants into cultivation: opportunities and challenges for biotechnology. Trends Biotechnol 23:180–185
Capelo AM, Silva S, Brito G, Santos C (2010) Somatic embryogenesis induction in leaves and petioles of a mature wild olive. Plant Cell Tissue Organ Cult 103:237–242
Caponetti JD, Gray DJ, Trigiano RN (2005) History of plant tissue and cell culture. In: Trigiano RN, Gray DJ (eds) Plant Development and Biotechnology. CRC Press, Florida, USA, pp 9–15
Carpentier AS, Abreu S, Trichet M, Satiat-Jeunemaitre B (2012) Microwaves and tea: new tools to process plant tissue for transmission electron microscopy. J Microsc 247:94–105
Chakrabarty D, Park SY, Ali MB, Shin KS, Paek KY (2006) Hyperhydricity in apple: ultrastructural and physiological aspects. Tree Physiol 26:377–388
Chalfie M, Kain SR (2005) Methods of biochemical analysis, green fluorescent protein: properties, applications and protocols, vol 47. Wiley-Interscience, New Jersey
Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805
Chandler DE, Roberson RW (2009) Bioimaging: current concepts in light and electron microscopy. Jones and Bartlett Publishers, USA
Ckurshumova W, Caragea AE, Goldstein RS, Berleth T (2011) Glow in the dark: fluorescent proteins as cell and tissue-specific markers in plants. Mol Plant 4:794–804
Cole M, Jacobs B, Soubigou-Taconnat L, Balzergue S, Renou JP, Chandler JW, Werr W (2013) Live imaging of DORNRÖSCHEN and DORNRÖSCHEN-LIKE promoter activity reveals dynamic changes in cell identity at the microcallus surface of Arabidopsis embryonic suspensions. Plant Cell Rep 32:45–59
Correll MJ, Weathers PJ (2001) Effects of light, CO2 and humidity on carnation growth, hyperhydration and cuticular wax development in a mist reactor. In Vitro Cell Dev Biol-Plant 37:405–413
da Cruz ACF, Rocha DI, Iarema L, Ventrella MC, Costa MGC, Neto VBP, Otoni WC (2014) In vitro organogenesis from root culture segments of Bixa orellana L. (Bixaceae). In Vitro Cell Dev Biol-Plant 50:76–83
da Silva ML, Pinto DLP, Guerra MP, Floh ES, Bruckner CH, Otoni WC (2009) A novel regeneration system for a wild passion fruit species (Passiflora cincinnata Mast.) based on somatic embryogenesis from mature zygotic embryos. Plant Cell, Tissue Organ Cult 99:47–54
Dai J-L, Tan X, Zhan Y-G, Zhang Y-Q, Xiao S, Gao Y, Xu D-W, Wang T, Wang X-C, You X-L (2011) Rapid and repetitive plant regeneration of Aralia elata Seem. via somatic embryogenesis. Plant Cell, Tissue Organ Cult 104:125–130
Davidson MW, Campbell RE (2009) Engineered fluorescent proteins: innovations and applications. Nat Methods 6:713–717
De Boer HH, Van der Merwe AE, Maat GJR (2013) The diagnostic value of microscopy in dry bone palaeopathology: a review. Intl J Paleopathol 3:113–121
de Oliveira LM, Paiva R, de Santana JRF, Alves E, Nogueira RC, Pereira FD (2008) Effect of cytokinins on in vitro development of autotrophism and acclimatization of Annona glabra L. In Vitro Cell Dev Biol-Plant 44:128–135
Del Bianco M, Giustini L, Sabatini S (2013) Spatiotemporal changes in the role of cytokinin during root development. New Phytol 199:324–338
Demeter Z, Surányi G, Molnár VA, Sramkó G, Beyer D, Kónya Z, Vasas G, Hamvas M, Máthé C (2010) Somatic embryogenesis and regeneration from shoot primordia of Crocus heuffelianus. Plant Cell Tissue Organ Cult 100:349–353
Dewir Y, Singh N, Shaik S, Nicholas A (2010) Indirect regeneration of the Cancer bush (Sutherlandia frutescens L.) and detection of l-canavanine in in vitro plantlets using NMR. In Vitro Cell Dev Biol-Plant 46:41–46
Dobránszki J, Teixeira da Silva JA (2010) Micropropagation of apple—A review. Biotechnol Adv 28:462–488
Domozych DS (2012) The quest for four-dimensional imaging in plant cell biology: it’s just a matter of time. Ann Bot 110:461–474
El-Bakry M, Sheehan J (2014) Analysing cheese microstructure: a review of recent developments. J Food Eng 125:84–96
Fehér A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228
Follet-Gueye M-L, Pagny S, Faye L, Gomord V, Driouich A (2003) An improved chemical fixation method suitable for immunogold localization of green fluorescent protein in the Golgi apparatus of tobacco bright yellow (BY-2) cells. J Histochem Cytochem 51:931–940
Fontes MA, Otoni WC, Carolino SMB, Brommonschenkel SH, Fontes EPB, Fári M, Louro RP (1999) Hyperhydricity in pepper plants regenerated in vitro: involvement of BiP (Binding Protein) and ultrastructural aspects. Plant Cell Rep 19:81–87
George EF (1993) Plant propagation by tissue culture, part 1: the technology. Exegetics Ltd, London, UK
Grzebelus E, Szklarczyk M, Baranski R (2012) An improved protocol for plant regeneration from leaf- and hypocotyl-derived protoplasts of carrot. Plant Cell, Tissue Organ Cult 109:101–109
Guha S, Rao IU (2010) Culture surface and exogenous putrescine-altered shoot growth pattern in mannitol- and cadmium chloride-pretreated callus of Cymbidium Via del Playa “Yvonne”. In Vitro Cell Dev Biol-Plant 46:491–498
Gzyl J, Przymusiński R, Gwóźdź EA (2009) Ultrastructure analysis of cadmium-tolerant and -sensitive cell lines of cucumber (Cucumis sativus L.). Plant Cell, Tissue Organ Cult 99:227–232
Haseloff J, Siemering KR (2005) The uses of green fluorescent protein in plants. In: Green Fluorescent Protein. Wiley, pp 259–284. doi:10.1002/0471739499.ch12
Hashimoto T, Takahashi K, Sato M, Bandara PKGSS, Nabeta K (2011) Cloning and characterization of an allene oxide cyclase, PpAOC3, in Physcomitrella patens. Plant Growth Regul 65:239–245
Hazarika BN (2006) Morpho-physiological disorders in in vitro culture of plants. Sci Hortic 108:105–120
He Y, Guo X, Lu R, Niu B, Pasapula V, Hou P, Cai F, Xu Y, Chen F (2009) Changes in morphology and biochemical indices in browning callus derived from Jatropha curcas hypocotyls. Plant Cell Tissue Organ Cult 98:11–17
Holme IB, Brinch-Pedersen H, Lange M, Holm PB (2006) Transformation of barley (Hordeum vulgare L.) by Agrobacterium tumefaciens infection of in vitro cultured ovules. Plant Cell Rep 25:1325–1335
Hraška M, Rakouský S, Čurn V (2006) Green fluorescent protein as a vital marker for non-destructive detection of transformation events in transgenic plants. Plant Cell, Tissue Organ Cult 86:303–318
Huai J, Zheng J, Wang G (2009) Overexpression of a new Cys2/His2 zinc finger protein ZmZF1 from maize confers salt and drought tolerance in transgenic Arabidopsis. Plant Cell Tissue Organ Cult 99:117–124
Huang C-H, Chung J-P (2011) Efficient indirect induction of protocorm-like bodies and shoot proliferation using field-grown axillary buds of a Lycaste hybrid. Plant Cell Tissue Organ Cult 106:31–38
Iliev I, Kitin P (2011) Origin, morphology, and anatomy of fasciation in plants cultured in vivo and in vitro. Plant Growth Regul 63:115–129
Ivanova M, Van Staden J (2010) Natural ventilation effectively reduces hyperhydricity in shoot cultures of Aloe polyphylla Schönland ex Pillans. Plant Growth Regul 60:143–150
Jahn KA, Barton DA, Kobayashi K, Ratinac KR, Overall RL, Braet F (2012) Correlative microscopy: providing new understanding in the biomedical and plant sciences. Micron 43:565–582
Jausoro V, Llorente BE, Apóstolo NM (2010a) Structural differences between hyperhydric and normal in vitro shoots of Handroanthus impetiginosus (Mart. ex DC) Mattos (Bignoniaceae). Plant Cell Tissue Organ Cult 101:183–191
Jausoro V, Llorente BE, Apóstolo NM (2010b) Structural differences between hyperhydric and normal in vitro shoots of Handroanthus impetiginosus (Mart. ex DC) Mattos (Bignoniaceae). Plant Cell, Tissue Organ Cult 101:183–191
Juszczyk J, Krzywiecki M, Kruszka R, Bodzenta J (2013) Application of scanning thermal microscopy for investigation of thermal boundaries in multilayered photonic structures. Ultramicroscopy 135:95–98
Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43:179–188
Kajikawa K, Yamaguchi T, Katsuda S, Miwa A (1975) An improved electron stain for elastic fibers using tannic acid. J Electron Microsc 24:287–289
Kane ME (2005) Shoot culture procedures. In: Trigiano RN, Gray DJ (eds) Plant Development and Biotechnology. CRC Press, Washington D.C. USA
Kang YM, Park DJ, Min JY, Song HJ, Jeong MJ, Kim YD, Kang SM, Karigar CS, Choi MS (2011) Enhanced production of tropane alkaloids in transgenic Scopolia parviflora hairy root cultures over-expressing putrescine N-methyl transferase (PMT) and hyoscyamine-6β-hydroxylase (H6H). In Vitro Cell Dev Biol-Plant 47:516–524
Karuppusamy S (2009) A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plant Res 3:1222–1239
Kozai T (1991) Photoautotrophic micropropagation. In Vitro Cell Dev Biol-Plant 27:47–51
Kozai T, Kubota C, Ryoung Jeong B (1997) Environmental control for the large-scale production of plants through in vitro techniques. Plant Cell Tissue Organ Cult 51:49–56
Kuo J (2007) Electron microscopy: Methods and protocols, vol 369. Humana Press Inc., New Jersey, USA
Kurczyńska EU, Gaj MD, Ujczak A, Mazur E (2007) Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh. Planta 226:619–628
Lai K, Yusoff K, Mahmood M (2013) Functional ectodomain of the hemagglutinin-neuraminidase protein is expressed in transgenic tobacco cells as a candidate vaccine against Newcastle disease virus. Plant Cell Tissue Organ Cult 112:117–121
Larkin P, Scowcroft W (1981) Somaclonal variation—A novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214
Lin G-Z, Zhao X-M, Hong S-K, Lian Y-J (2011) Somatic embryogenesis and shoot organogenesis in the medicinal plant Pulsatilla koreana Nakai. Plant Cell Tissue Organ Cult 106:93–103
Liu X, Sun L, Li C, Yang A, Zhang J (2013) Enhanced expression of the human CD14 protein in tobacco using a 22-kDa alpha-zein signal peptide. Plant Cell Tissue Organ Cult 112:9–18
López-Villalobos A, Dodds PF, Hornung R (2011) Lauric acid improves the growth of zygotic coconut (Cocos nucifera L.) embryos in vitro. Plant Cell Tissue Organ Cult 106:317–327
Mathur J (2007) The illuminated plant cell. Trends in Plant Sci 12:506–513
Mayer JLS, Stancato GC, Appezzato-Da-Glória B (2010) Direct regeneration of protocorm-like bodies (PLBs) from leaf apices of Oncidium flexuosum Sims (Orchidaceae). Plant Cell Tissue Organ Cult 103:411–416
Mendes MD, Cristina Figueiredo A, Margarida Oliveira M, Trindade H (2013) Essential oil production in shoot cultures versus field-grown plants of Thymus caespititius. Plant Cell Tissue Organ Cult 113:341–351
Mondal TK, Bhattacharya A, Laxmikumaran M, Singh Ahuja P (2004) Recent advances of tea (Camellia sinensis) biotechnology. Plant Cell Tissue Organ Cult 76:195–254
Motte H, Vereecke D, Geelen D, Werbrouck S (2014) The molecular path to in vitro shoot regeneration. Biotechnol Adv 32:107–121
Moyo M, Finnie JF, Van Staden J (2009) In vitro morphogenesis of organogenic nodules derived from Sclerocarya birrea subsp. caffra leaf explants. Plant Cell Tissue Organ Cult 98:273–280
Moyo M, Bairu MW, Amoo SO, Van Staden J (2011) Plant biotechnology in South Africa: micropropagation research endeavours, prospects and challenges. S Afr J Bot 77:996–1011
Moyo M, Finnie JF, Van Staden J (2012) Topolins in Pelargonium sidoides micropropagation: do the new brooms really sweep cleaner? Plant Cell Tissue Organ Cult 110:319–327
Moyo M, Koetle MJ, Van Staden J (2014) Photoperiod and plant growth regulator combinations influence growth and physiological responses in Pelargonium sidoides DC. In Vitro Cell Dev Biol-Plant 50:487–492
Muday GK, DeLong A (2001) Polar auxin transport: controlling where and how much. Trends in Plant Sci 6:535–542
Murphy DB, Davidson MW (2013) Fundamentals of light microscopy and electronic imaging, 2nd edn. Wiley-Blackwell, New Jersey, USA
Nakagawa R, Kurushima M, Matsui M, Nakamura R, Kubo T, Funada R (2011) Polyamines promote the development of embryonal-suspensor masses and the formation of somatic embryos in Picea glehnii. In Vitro Cell Dev Biol-Plant 47:480–487
Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-Go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1141
Neelakandan A, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620
Nogué F, Grandjean O, Craig S, Dennis S, Chaudhury M (2000) Higher levels of cell proliferation rate and cyclin CycD3 expression in the Arabidopsis amp1 mutant. Plant Growth Regul 32:275–283
Olmos E, Hellín E (1998) Ultrastructural differences of hyperhydric and normal leaves from regenerated carnation plants. Sci Hortic 75:91–101
Parra-Vega V, Renau-Morata B, Sifres A, Seguí-Simarro JM (2013) Stress treatments and in vitro culture conditions influence microspore embryogenesis and growth of callus from anther walls of sweet pepper (Capsicum annuum L.). Plant Cell Tissue Organ Cult 112:353–360
Pavlović S, Vinterhalter B, Zdravković-Korać S, Vinterhalter D, Zdravković J, Cvikić D, Mitić N (2013) Recurrent somatic embryogenesis and plant regeneration from immature zygotic embryos of cabbage (Brassica oleracea var. capitata) and cauliflower (Brassica oleracea var. botrytis). Plant Cell Tissue Organ Cult 113:397–406
Pavoković D, Poljuha D, Horvatić A, Ljubešić N, Hagège D, Krsnik-Rasol M (2012) Morphological and proteomic analyses of sugar beet cultures and identifying putative markers for cell differentiation. Plant Cell Tissue Organ Cult 108:111–119
Pence VC (2010) The possibilities and challenges of in vitro methods for plant conservation. Kew Bull 65:539–547
Picas L, Milhiet P-E, Hernández-Borrell J (2012) Atomic force microscopy: a versatile tool to probe the physical and chemical properties of supported membranes at the nanoscale. Chem Phys Lipids 165:845–860
Picoli EAT, Otoni WC, MrL Figueira, Carolino SMB, Almeida RS, Silva EAM, Carvalho CR, Fontes EPB (2001) Hyperhydricity in in vitro eggplant regenerated plants: structural characteristics and involvement of BiP (Binding Protein). Plant Sci 160:857–868
Pospíšilová J, Synková H, Haisel D, Semorádová S (2007) Acclimation of plantlets to ex vitro conditions: effects of air humidity, irradiance, CO2 concentration and abscisic acid (a review). Acta Hortic 748:29–38
Potocka I, Baldwin TC, Kurczynska EU (2012) Distribution of lipid transfer protein 1 (LTP1) epitopes associated with morphogenic events during somatic embryogenesis of Arabidopsis thaliana. Plant Cell Rep 31:2031–2045
Prasher DC, Eckenrode VK, Ward WW, Prendergast FG, Cormier MJ (1992) Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111:229–233
Ptak A, Tahchy AE, Wyżgolik G, Henry M, Laurain-Mattar D (2010) Effects of ethylene on somatic embryogenesis and galanthamine content in Leucojum aestivum L. cultures. Plant Cell Tissue Organ Cult 102:61–67
Qi Y, Lou Q, Quan Y, Liu Y, Wang Y (2013) Flower-specific expression of the Phalaenopsis flavonoid 3′, 5′-hydroxylase modifies flower color pigmentation in Petunia and Lilium. Plant Cell Tissue Organ Cult 115:263–273
Quiala E, Cañal M-J, Meijón M, Rodríguez R, Chávez M, Valledor L, de Feria M, Barbón R (2012) Morphological and physiological responses of proliferating shoots of teak to temporary immersion and BA treatments. Plant Cell Tissue Organ Cult 109:223–234
Raju SC, Kathiravan K, Aslam A, Shajahan A (2013) An efficient regeneration system via somatic embryogenesis in mango ginger (Curcuma amada Roxb.). Plant Cell, Tissue Organ Cult 112:387–393
Ramachandra Rao S, Ravishankar GA (2002) Plant cell cultures: chemical factories of secondary metabolites. Biotechnol Adv 20:101–153
Ramakrishna A, Giridhar P, Ravishankar GA (2011) Calcium and calcium ionophore A23187 induce high-frequency somatic embryogenesis in cultured tissues of Coffea canephora P ex Fr. In Vitro Cell Dev Biol-Plant 47:667–673
Ramakrishna A, Giridhar P, Jobin M, Paulose CS, Ravishankar GA (2012) Indoleamines and calcium enhance somatic embryogenesis in Coffea canephora P ex Fr. Plant Cell, Tissue Organ Cult 108:267–278
Redha A, Suleman P (2011) Effects of exogenous application of polyamines on wheat anther cultures. Plant Cell Tissue Organ Cult 105:345–353
Reichel C, Mathur J, Eckes P, Langenkemper K, Koncz C, Schell J, Reiss B, Maas C (1996) Enhanced green fluorescence by the expression of an Aequorea victoria green fluorescent protein mutant in mono- and dicotyledonous plant cells. Proc Natl Acad Sci USA 93:5888–5893
Roberts WS, Lonsdale DJ, Griffiths J, Higson SPJ (2007) Advances in the application of scanning electrochemical microscopy to bioanalytical systems. Biosens Bioelectron 23:301–318
Rocha DI, Vieira LM, Tanaka FAO, da Silva LC, Otoni WC (2012) Anatomical and ultrastructural analyses of in vitro organogenesis from root explants of commercial passion fruit (Passiflora edulis Sims). Plant Cell Tissue Organ Cult 111:69–78
Rojas-Martínez L, Visser RGF, de Klerk G-J (2010) The hyperhydricity syndrome: waterlogging of plant tissues as a major cause. Propag Ornam Plant 10:169–175
Rosa YBCJ, Dornelas MC (2012) In vitro plant regeneration and de novo differentiation of secretory trichomes in Passiflora foetida L. (Passifloraceae). Plant Cell Tissue Organ Cult 108:91–99
Rosa YBC, Aizza LCB, Armanhi JSL, Dornelas MC (2013) A Passiflora homolog of a D-type cyclin gene is differentially expressed in response to sucrose, auxin, and cytokinin. Plant Cell Tissue Organ Cult 115:233–242
Rout GR, Samantaray S, Das P (2000) In vitro manipulation and propagation of medicinal plants. Biotechnol Adv 18:91–120
Rout GR, Mohapatra A, Jain SM (2006) Tissue culture of ornamental pot plant: a critical review on present scenario and future prospects. Biotechnol Adv 24:531–560
Ruffoni B, Savona M (2013) Physiological and biochemical analysis of growth abnormalities associated with plant tissue culture. Hortic Environ Biotechnol 54:191–205
Rugkhla A, Jones MGK (1998) Somatic embryogenesis and plantlet formation in Santalum album and S. spicatum. J Exp Bot 49:563–571
Sáenz L, Azpeitia A, Chuc-Armendariz B, Chan JL, Verdeil JL, Hocher V, Oropeza C (2006) Morphological and histological changes during somatic embryo formation from coconut plumule explants. In Vitro Cell Dev Biol-Plant 42:19–25
Sato S, Adachi A, Sasaki Y, Ghazizadeh M (2008) Oolong tea extract as a substitute for uranyl acetate in staining of ultrathin sections. J Microsc 229:17–20
Sharifi G, Ebrahimzadeh H, Ghareyazie B, Karimi M (2010) Globular embryo-like structures and highly efficient thidiazuron-induced multiple shoot formation in saffron (Crocus sativus L.). In Vitro Cell Dev Biol-Plant 46:274–280
Shimomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59:223–239
Shur J, Price R (2012) Advanced microscopy techniques to assess solid-state properties of inhalation medicines. Adv Drug Deliver Rev 64:369–382
Sirerol-Piquer MS, Cebrián-Silla A, Alfaro-Cervelló C, Gomez-Pinedo U, Soriano-Navarro M, Verdugo J-MG (2012) GFP immunogold staining, from light to electron microscopy, in mammalian cells. Micron 43:589–599
Sivanesan I, Song JY, Hwang SJ, Jeong BR (2011) Micropropagation of Cotoneaster wilsonii Nakai—a rare endemic ornamental plant. Plant Cell Tissue Organ Cult 105:55–63
Smith-Espinoza C, Bartels D, Phillips J (2007) Analysis of a LEA gene promoter via Agrobacterium-mediated transformation of the desiccation tolerant plant Lindernia brevidens. Plant Cell Rep 26:1681–1688
Smulders M, de Klerk G (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63:137–146
Sreedhar RV, Venkatachalam L, Neelwarne B (2009) Hyperhydricity-related morphologic and biochemical changes in vanilla (Vanilla planifolia). J Plant Growth Regul 28:46–57
Steiner N, Santa-Catarina C, Guerra MP, Cutri L, Dornelas MC, Floh ES (2012) A gymnosperm homolog of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE-1 (SERK1) is expressed during somatic embryogenesis. Plant Cell Tissue Organ Cult 109:41–50
Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci 98:11806–11811
Sun X, Ji W, Ding X, Bai X, Cai H, Yang S, Qian X, Sun M, Zhu Y (2013) GsVAMP72, a novel Glycine soja R-SNARE protein, is involved in regulating plant salt tolerance and ABA sensitivity. Plant Cell Tissue Organ Cult 113:199–215
Tang W, Newton RJ, Charles TM (2005) High efficiency inducible gene expression system based on activation of a chimeric transcription factor in transgenic pine. Plant Cell Rep 24:619–628
Teixeira da Silva JA (2003) Chrysanthemum: advances in tissue culture, cryopreservation, postharvest technology, genetics and transgenic biotechnology. Biotechnol Adv 21:715–766
Tewari RK, Prommer J, Watanabe M (2013) Endogenous nitric oxide generation in protoplast chloroplasts. Plant Cell Rep 32:31–44
Thomasson MS, Macnaughtan MA (2013) Microscopy basics and the study of actin–actin-binding protein interactions. Anal Biochem 443:156–165
Torrealba F, Carrasco MA (2004) A review on electron microscopy and neurotransmitter systems. Brain Res Rev 47:5–17
Tranfield EM, Walker DC (2013) The ultrastructure of animal atherosclerosis: what has been done, and the electron microscopy advancements that could help scientists answer new biological questions. Micron 46:1–11
Trigiano RN, Malueg KR, Pickens KA, Cheng Z-M, Graham ET (2005) Histological techniques. In: Trigiano RN, Gray DJ (eds) Plant Development and Biotechnology. CRC Press, Boca Raton, Florida, USA, pp 39–54
Valero-Aracama C, Kane M, Wilson S, Vu J, Anderson J, Philman N (2006) Photosynthetic and carbohydrate status of easy-and difficult-to-acclimatize sea oats (Uniola paniculata L.) genotypes during in vitro culture and ex vitro acclimatization. In Vitro Cell Dev Biol-Plant 42:572–583
Van Eck J, Keen P (2009) Continued expression of plant-made vaccines following long-term cryopreservation of antigen-expressing tobacco cell cultures. In Vitro Cell Dev Biol-Plant 45:750–757
Vasil I (2008) A history of plant biotechnology: from the cell theory of Schleiden and Schwann to biotech crops. Plant Cell Rep 27:1423–1440
Verpoorte R, Memelink J (2002) Engineering secondary metabolite production in plants. Curr Opin Biotech 13:181–187
Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12:160–168
Wakte KV, Nadaf AB, Thengane RJ, Jawali N (2009) In vitro regenerating plantlets in Pandanus amaryllifolius Roxb. as a model system to study the development of lower epidermal papillae. In Vitro Cell Dev Biol-Plant 45:701–707
Werker E, Leshem B (1987) Structural changes during vitrification of carnation plantlets. Ann Bot 59:377–385
Whited AM, Park PSH (2014) Atomic force microscopy: a multifaceted tool to study membrane proteins and their interactions with ligands. Biochim Bioph Acta- Biomembranes 1838:56–68
Woo SM, Wetzstein HY (2008) Morphological and histological evaluations of in vitro regeneration in Elliottia racemosa leaf explants induced on media with thidiazuron. J Am Soc Hortic Sci 133:167–172
Wu Z, Chen LJ, Long YJ (2009) Analysis of ultrastructure and reactive oxygen species of hyperhydric garlic (Allium sativum L.) shoots. In Vitro Cell Dev Biol-Plant 45:483–490
Wu J-J, Liu Y-W, Sun M-X (2011) Improved and high throughput quantitative measurements of weak GFP expression in transgenic plant materials. Plant Cell Rep 30:1253–1260
Xu X, Guo R, Cheng C, Zhang H, Zhang Y, Wang X (2013) Overexpression of ALDH2B8, an aldehyde dehydrogenase gene from grapevine, sustains Arabidopsis growth upon salt stress and protects plants against oxidative stress. Plant Cell, Tissue Organ Cult 114:187–196
Yang Y, Yang L, Li Z (2013) Molecular cloning and identification of a putative tomato cationic amino acid transporter-2 gene that is highly expressed in stamens. Plant Cell, Tissue Organ Cult 112:55–63
Zacharias DA, Tsien RY (2005) Molecular biology and mutation of green fluorescent protein. In: Green Fluorescent Protein. Wiley, pp 83–120. doi:10.1002/0471739499.ch5
Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5:1411–1423
Ziv M (1991) Vitrification: morphological and physiological disorders of in vitro plants. In: Debergh PC, Zimmerman RH (eds) Micropropagation: Technology and Applications. Kluwer Academic Publishers, Dordrecht, pp 45–69
Zumbusch A, Langbein W, Borri P (2013) Nonlinear vibrational microscopy applied to lipid biology. Prog Lipid Res 52:615–632
Acknowledgments
The authors gratefully acknowledge financial support from Claude Leon Foundation, the University of KwaZulu-Natal and National Research Foundation, South Africa. We thank Dr W.A. Stirk for her valuable suggestions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Moyo, M., Aremu, A.O. & Van Staden, J. Insights into the multifaceted application of microscopic techniques in plant tissue culture systems. Planta 242, 773–790 (2015). https://doi.org/10.1007/s00425-015-2359-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-015-2359-4