Plant Cell Tiss Organ Cult (2011) 106:179–190 DOI 10.1007/s11240-011-9923-9
REVIEW
The role of abscisic acid in plant tissue culture: a review of recent progress Manoj K. Rai • N. S. Shekhawat • Harish • Amit K. Gupta • M. Phulwaria • Kheta Ram U. Jaiswal
•
Received: 17 October 2010 / Accepted: 17 January 2011 / Published online: 5 February 2011 Ó Springer Science+Business Media B.V. 2011
Abstract Abscisic acid (ABA) plays a significant role in the regulation of many physiological processes of plants. It is often used in tissue culture systems to promote somatic embryogenesis and enhance somatic embryo quality by increasing desiccation tolerance and preventing precocious germination. ABA is also employed to induce somatic embryos to enter a quiescent state in plant tissue culture systems and during synthetic seed research. Application of exogenous ABA improves in vitro conservation and the adaptive response of plant cell and tissues to various environmental stresses. ABA can act as anti-transpirant during the acclimatization of tissue culture-raised plantlets and reduces relative water loss of leaves during the ex vitro transfer of plantlets even when non-functional stomata are present. This review focuses on the possible roles of ABA in plant tissue culture and recent developments in this area. Keywords Acclimatization Anti-transpirant Cryopreservation Embryo maturation Plant growth regulator Somatic embryogenesis
The work is dedicated to the first author’s late supervisor Prof. V.S. Jaiswal (1945–2007). M. K. Rai (&) N. S. Shekhawat Harish A. K. Gupta M. Phulwaria K. Ram U. Jaiswal Department of Botany, Biotechnology Centre, Jai Narain Vyas University, Jodhpur, Rajasthan 342033, India e-mail:
[email protected] U. Jaiswal Department of Botany, Mahila Mahavidyalaya, Banaras Hindu University, Varanasi, Uttar Pradesh 221005, India
Introduction The growth of plant organs depends mainly on a combination of cell division and cell expansion, which is highly regulated by environmental factors, such as light, temperature etc. and by endogenous factors, such as phytohormones. The sequential coordination of multiple cellular processes is also one of the important components of the processes involved in the growth regulation of plant organs under specific situations, including nutritional status, developmental stage and abiotic stress (Alabadi and Blazquez 2009). When the appropriate growth stimulus is perceived, all of the different cell types and tissues respond synchronously (Savaldi-Goldstein et al. 2007; Ubeda-Tomas et al. 2008; Alabadi and Blazquez 2009). However, under in vitro conditions, explants have been removed from their original tissue environment and transferred to synthetic media containing non-physiological concentrations of growth regulators and organic and inorganic constituents, resulting in exposure to significant stresses. Under extreme conditions, the developmental program of plants is highly flexible, and this adaptability is directly associated with the capability of somatic plant cells to reverse the differentiation process. Plant growth regulators (PGRs) are considered to be the most important factors involved in the regulation of these developmental switches under in vitro conditions (Feher et al. 2003). Auxins, cytokinins, gibberellins, abscisic acid and ethylene are commonly recognized as naturally occurring plant hormones. Among these, auxins and cytokinins are mostly employed in plant tissue culture systems to regulate cell division and differentiation in the explants. However, other PGRs and a number of new natural growth substances, such as polyamines, jasmonates, brassinosteroids, oligosaccharins, sterols, phosphoinositosides and salicylic acid, also have specific regulatory roles
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which must not be ignored in culture systems (Gaspar et al. 1996; Jimenez 2005). During the 1960s, researchers isolated a compound from cotton bolls which was identified as an abscission factor (denoted abscisin II) (Ohkuma et al. 1963). During this same period, Cornforth et al. (1965) were successful in isolating a compound from sycamore leaves, denoted dormin, that proved to be involved in bud dormancy. A comparative analysis of the chemical structures of these two compounds by infrared spectroscopy revealed that they were one and the same compound (Addicott et al. 1968) and, following its purification and determination of its chemical structure, this compound was renamed abscisic acid (ABA). Subsequent studies revealed that the ABA level increases considerably when plants wilt (Wright and Hiron 1969) and that ABA causes stomatal closure (Mittelheuser and Van Steveninck 1969). These two discoveries highlighted the involvement of ABA in the plant’s response to abiotic stress (Milborrow 2001; Mongrand et al. 2003) and resulted in considerable research efforts focusing on various aspects of the involvement of ABA in tolerance to environmental stress, stomatal closure, desiccation tolerance and dormancy induction in seeds (Bewley 1997; Finkelstein et al. 2002, 2008; Mongrand et al. 2003; Tuteja 2007; Tuteja and Sopory 2008). During the last 20–30 years, ABA has attracted the interest of many plant tissue culture specialists due to the significant role it plays in desiccation tolerance and maturation of somatic embryos, synthetic seed research, cryopreservation procedures and anti-transpirant effect during the acclimatization of tissue cultureraised plants. This review focuses on the role of ABA in various morphological and physiological processes, with a specific focus on plant tissue culture. Recent developments are also emphasized.
Biosynthesis and functions of ABA in higher plants Abscisic acid, a sesquiterpenoid (15-carbon), is commonly synthesized in all vascular plants, but it is also present in mosses and all algal classes, including photosynthetic prokaryotes, such as cyanobacteria. Some pathogenic fungi also synthesize ABA, but the biosynthetic pathway in fungi is quite different from that in higher plants (Mongrand et al. 2003; Schwartz et al. 2003). In plant cells, ABA is generally maintained at low levels under non-stressful conditions, as it may be required for normal plant growth. However, ABA levels can increase significantly in response to environmental stresses and during seed maturation (Xiong and Zhu 2003). ABA is synthesized in almost all cells containing chloroplasts or amyloplasts (Mongrand et al. 2003). Normally, different
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parts of the plant synthesize ABA according to their physiological requirements, and their regulatory controls appear to be different. For example, as plant tissues lose water, the amount of ABA increases progressively in the roots, and this compound is therefore translocated to other parts of the plant, while during wilting, the leaves respond by inducing a rapid and increased synthesis of ABA. Seeds synthesize ABA during maturation, which stimulates the accumulation of storage reserves and induces seed dormancy (Milborrow 2001). Many papers have been published during the last 20 years on the regulation of ABA biosynthesis (Liotenberg et al. 1999; Milborrow 2001; Finkelstein et al. 2002; Schwartz et al. 2003; Xiong and Zhu 2003; Tuteja 2007; Chinnusamy et al. 2008). As a result, the biosynthesis pathway for ABA in higher plants is now understood, and many of the genes encoding enzymes involved in this process have been identified (Schwartz et al. 2003; Xiong and Zhu 2003). In higher plants, ABA is synthesized through an ‘‘indirect’’ pathway via the oxidative cleavage of a 9-cis-epoxycarotenoid (C40) to produce xanthoxin (C15) in the plastids, followed by a two-step conversion of the intermediate xanthoxin to ABA via ABA-aldehyde in the cytoplasm (Fig. 1; Schwartz et al. 2003; Xiong and Zhu 2003). Epoxidation of zeaxanthin and antheraxanthin (9-cis-epoxicarotenoid precursors) to violaxanthin is the first step in the ABA biosynthetic pathway and is catalyzed by a zeaxanthin epoxidase (ZEP). Violaxanthin is modified structurally by cis-isomerases and converted to 9-cis-epoxycarotenoids. 9-cis-neoxanthin, a major 9-cis-epoxicarotenoid, is catalyzed by 9-cis-epoxicarotenoid dioxygenase (NCED) to produce a C15 intermediate, xanthoxin (Schwartz et al. 1997, 2003; Xiong and Zhu 2003). The xanthoxin is then exported to the cytosol, where it is converted to ABA-aldehyde by a short-chain alcohol dehydrogenase/reductase (SDR). In the last step of the pathway, ABA-aldehyde is oxidized to ABA by ABA-aldehyde oxidase (AAO; Xiong and Zhu 2003). ABA biosynthetic genes, namely, ZEP, NCED and AAO, are up-regulated by abiotic stresses through a calcium-dependent phosphorylation pathway, whereas SDR is regulated by sugar (Fig. 1; Xiong and Zhu 2003; Tuteja 2007). The accumulation of ABA can also a feedback loop which stimulates the expression of genes involved in ABA biosynthesis through the calcium signaling pathway and to activate the ABA catabolic enzymes to degrade the ABA (Tuteja 2007). ABA plays a key role in many developmental processes, including the promotion of seed desiccation tolerance, maturation of embryos and seed development, seed dormancy and delay in germination, synthesis of storage proteins and lipids and organ senescence (Bewley 1997; Finkelstein et al. 2002, 2008; Mongrand et al. 2003; Schwartz et al. 2003; Xiong and Zhu 2003; Tuteja 2007;
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sm la ast β -Carotene (C40) p to opl y r C Zeaxanthin lo h ZEP C ZEP
Abiotic stresses
NCED
Violaxanthin
Sugar
Neoxanthin
cis isomerase
cis isomerase
9-cis-Violaxanthin
9-cis-Neoxanthin
NCED
NCED
AA O
Fig. 1 Biosynthetic pathways of abscisic acid (ABA) in plants (for more details, see Schwartz et al. 2003; Xiong and Zhu 2003). ZEP, AAO, NCED, SDR Genes coding for zeaxanthin epoxidase, ABA-aldehyde oxidase, 9-cis-epoxicarotenoid dioxygenase, short-chain alcohol dehydrogenase/ reductase, respectively
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SD R
AAO
ABA
NCED
SDR
ABA-aldehyde
Xanthoxin (C15)
ABA biosynthetic genes (ZEP, NCED, AAO) upregulated by abiotic stresses ABA biosynthetic genes (SDR) upregulated by sugar
Tuteja and Sopory 2008; Table 1). In addition, ABA acts as an endogenous messenger in the regulation of plantwater status (Tuteja 2007), and regulates some aspects of the plant’s physiological responses to environmental stresses, such as osmotic stress-induced stomatal closure and salt, drought and cold tolerance (Mongrand et al. 2003; Schwartz et al. 2003; Xiong and Zhu 2003; Tuteja 2007). Because different stresses induce the accumulation of endogenous ABA, it is now referred to as a plant stress hormone (Tuteja 2007; Tuteja and Sopory 2008). Recent results demonstrate that ABA can also act in increasing the resistance of plants towards pathogens (Mauch-Mani and Mauch 2005; Fan et al. 2009).
Role of ABA in plant tissue culture Although ABA participates in the regulation of many physiological processes of whole plants (Tuteja 2007), it is regarded as an inhibitor of plant growth and therefore usually used as a growth retardant in plant tissue culture (Engelmann 1991; Sharp et al. 2000; Rai et al. 2009a). However, various authors have pointed out that while exogenous ABA alone suppresses shoot regeneration, when added to a plant culture system in combination with other PGRs, it has a promoting effect (Sen et al. 1989; Ficcadenti and Rotino 1995; Maggon and Singh 1995). To date, ABA has been primarily used in plant tissue culture studies to
Table 1 Possible roles of absicisic acid (ABA) in plants/plant tissue culture Cell level
Whole plant level
Plant tissue culture level
Inhibition of cell division and cell elongation
Promotes seed desiccation tolerance
Promotes desiccation tolerance and the maturation of somatic embryos
Biosynthesis of storage proteins and fatty acids required for seed germination
Maturation of zygotic embryos and Inhibits precocious germination of seed development somatic embryos
Acts as endogenous messenger in the regulation of the plant’s water status and plays an important role in stomata closure
Seed dormancy and delays germination
Regulates synthesis of storage proteins in somatic embryos
Induction of tolerance to salt, drought and cold stress
Synchronization of somatic embryos
Employed in increasing the resistance of plants towards pathogens
Growth retardant/involved in slowgrowth of cultures
Organ senescence
Increased stress tolerance Acts as anti-transpirant in acclimatization of tissue culture raised plantlets
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promote the maturation of somatic embryos and the synthesis of storage reserves in embryos during maturation (Dodeman et al. 1997; von Arnold et al. 2002; Chugh and Khurana 2002). ABA also acts as a controlling factor of germination and dormancy in somatic embryos (Ara et al. 1999) and is generally used to induce somatic embryos into a quiescent state during plant tissue culture and synthetic seed studies (Zimmermann 1993; Rai et al. 2008a). In addition, ABA can be used as an anti-transpirant during the acclimatization of tissue culture-raised plants (Pospisilova et al. 1999). Table 2 provides a summary of the applications of ABA in plant tissue culture studies with special reference to recent reports (published in the last 4–5 years).
Somatic embryogenesis Somatic embryogenesis is an inductive process in which a competent cell or cell group undergoes a series of biochemical and molecular changes that result in the formation of a bipolar somatic embryo. Somatic embryogenesis is not only important for the production of large numbers of complete and uniform plants but also, integrated with molecular and cell biological techniques, it provides a valuable tool to enhance the pace of genetic improvement of many commercially important plants (Stasolla and Yeung 2003; Quiroz-Figueroa et al. 2006; Rai et al. 2010). The initiation of somatic embryogenesis is restricted only to certain competent cells that have the ability to activate those genes responsible for embryogenesis, and competence for somatic embryogenesis induction may be the result of variations in the sensitivity of competent cells to PGRs (Dudits et al. 1995; von Arnold et al. 2002; Rai et al. 2007, 2010). The role of exogenously applied auxins, mainly 2, 4-dichlorophenoxyacetic acid (2, 4-D), in the induction of somatic embryogenesis in many plants is well documented (von Arnold et al. 2002; Feher et al. 2003). Generally, ABA is found to inhibit the induction of somatic embryogenesis. However, carrot forms an exceptional case in that seedlings (with hypocotyls \30 mm in length) form somatic embryos directly when cultured on medium containing ABA as the sole PGR (Nishiwaki et al. 2000). One of the main explanations provided for this induction of somatic embryos in the presence of exogenous ABA is the increased level of endogenous auxins in shoot apices, the main source of auxins in seedlings. Charriere et al. (1999) also reported that in sunflower the level of endogenous indole-3-acetic acid increased following the application of ABA to immature zygotic embryos and resulted in the induction of somatic embryogenesis. Some reports postulate that the induction of somatic embryogenesis is sometimes regulated by the interaction of exogenous PGRs with
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various concentrations of endogenous hormones (Gaspar et al. 1996; Jimenez 2005). A number of factors limit the conversion of embryos into plants, of which the most important are considered to be a poor quality and incomplete maturation of somatic embryos and the germination of premature somatic embryos (Ammirato 1987; Choi and Jeong 2002; Choudhary et al. 2009; Rai et al. 2009b). During maturation, several storage and late embryogenesis abundant (LEA) proteins, fatty acid reserves and sugars, all required for germination, are synthesized, and mature somatic embryos, which have accumulated enough storage materials, develop into normal plants (von Arnold et al. 2002; Sharma et al. 2004). It is now well understood that both the synthesis and deposition of these storage and LEA proteins during somatic embryogenesis are regulated by ABA and stress-induced gene expression (Dodeman et al. 1997; Chugh and Khurana 2002; von Arnold et al. 2002). Raffinose oligosaccharides (ROs), which participate in the storage and transport of carbon, are stored in high amounts in the seeds of many plant species and are thought to have an important function in desiccation tolerance (Hannah et al. 2006). To establish a relationship between the accumulation of ROs and endogenous ABA, Blochl et al. (2005) treated alfalfa somatic embryos with different concentrations of ABA and analyzed the induction of enzymes of the RO pathways and the accumulation of sugars. These researchers found that the accumulation of two main ROs, namely, raffinose and stachyose, was highly dependent on the concentration of applied exogenous ABA. Sharma et al. (2004) also studied the effect of exogenous ABA on the accumulation of reserves (e.g., total soluble sugar, levels of starch, total proteins and phenols) during different stages of somatic embryos of Camellia sinensis and established a correlation between the accumulation of reserves and embryo maturation. More recently, Kharenko et al. (2011) also reported the induction of lipid accumulation in a seedling-derived suspension culture of Lesquerella fendleri following exogenous application of ABA. ABA not only promotes the transition of somatic embryos from the proliferation to the maturation phase (Langhansova et al. 2004), but it has also been used to enhance embryo quality by increasing desiccation tolerance and preventing precocious germination (Ammirato 1977; Senaratna et al. 1989; Attree et al. 1990; Lecouteux et al. 1993; Capuana and Debergh 1997; Li et al. 1997; Robichaud et al. 2004; Vahdati et al. 2008; Rai et al. 2008a; Fig. 2). ABA is also used to reduce the process of secondary embryogenesis (von Arnold et al. 2002). The synthesis of storage proteins during somatic embryo maturation is also greatly associated with changes in nitrogen
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Table 2 The role of ABA in plant tissue culture systems: recent studies Plant species
Role of ABA
References Barreto et al. (2010)
Agave tequilana
Increased production of ramets
Begonia x erythrophylla
Higher survival of cryopreserved shoots when pretreated with ABA
Burritt (2008)
Daucus carota
Involved in acquisition of embryogenic competence
Kikuchi et al. (2006)
Induction of dormancy and desiccation tolerance in somatic embryos
Shiota and Kamada (2008)
Ditrichum plumbicola (a threatened moss)
Induced the formation of highly desiccation and cryopreservation tolerant propagules from the protonemata
Rowntree et al. (2007)
Eucalyptus camaldulensis
Maturation of somatic embryos
Prakash and Gurumurthi (2010)
Ginkgo biloba
Post-cryopreservation survival of callus clump and accumulation of soluble sugar
Popova et al. (2009)
Juglans regia (Persian walnut)
Maturation and germination of somatic embryos
Vahdati et al. (2008)
Larix leptolepis (Japanese larch)
Maturation of somatic embryos and increased plantlet conversion
Kim and Moon (2007)
Lesquerella fendleri (Fendler’s bladderpod)
Induction of lipid accumulation in the seedling-derived suspension culture
Kharenko et al. (2011)
Malus domestica (apple)
In vitro cold storage of apple germplasm
Kovalchuk et al. (2009)
Medicago sativa
Act as regulators of ethylene biosynthesis during somatic embryogenesis
Ke˛pczynska et al. (2009)
Musa sp. (Plantain)
Maturation of somatic embryos Maturation of somatic embryos
Nicotiana tabacum
Improvement of ex vitro transfer of plantlets by addition to last subculture
Rudus et al. (2006) Sholi et al. (2009) Pospı´silova et al. (2009)
Phoenix dactylifera (date palm)
Accumulation of storage proteins in somatic embryos
Sghaier et al. (2009)
Phragmites communis (reed)
Exogenous application of ABA alleviated the heat stress symptoms in the calluses of two ecotypes
Ding et al. (2010)
Picea abies (Norway spruce)
Maturation of somatic embryos and expression of the gene encoding transcription factor PaVP1
Fischerova et al. (2008)
Picea glauca (Moench)
Maturation of somatic embryos
Kong and von Aderkas (2007)
Voss x engelmanni Parry ex Emgelm. (Interior spruce)
Cryotolerance induced in immature embryos by a combined treatment of ABA Kong and von Aderkas and low temperature (2011)
Pinellia ternata
Promotion of proliferation of PLBs
Pinus brutia (Turkish red pine)
Maturation of somatic embryos
Yildirim et al. (2006)
Pinus sylvestris (Scots pine)
Maturation of somatic embryos and accumulation of storage proteins
Lelu-Walter et al. (2008)
Pinus taeda (loblolly pine)
Improved somatic embryo maturation by monitoring ABA-responsive gene expression
Vales et al. (2007)
Psidium guajava (guava)
Induction of quiescent state in encapsulated somatic embryos and maturation Rai et al. (2008a) of somatic embryos
Psoralea corylifolia
Embryogenic callus induction and subsequently development and germination Baskaran and of somatic embryos Jayabalan (2009)
Quercus suber (Oak)
Somatic embryo maturation
metabolism. Changes in nitrogen metabolism and in the levels of specific amino acids, followed by the accumulation of storage proteins in response to ABA (Stasolla et al. 2002), may also be involved in the maturation process of somatic embryos. According to another hypothesis (?)ABA is able to stimulate embryo maturation upon rapid conversion to phaseic and dehydro-phaseic acid (Dunstan
Liu et al. (2010)
Garcia-Martin et al. (2005)
et al. 1992; Stasolla et al. 2002). Zhang et al. (2010) recently reported the role of exogenously applied ABA on H2O2 content during different stages of embryo development, further suggesting that the promotion of somatic embryos is ABA-dependent. For many plants, ABA does not promote somatic embryo maturation when added alone to the culture medium; however, it has been found to be
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Exogenous ABA
Accumulation of endogenous ABA Somatic embryos
A
B beneficial when used in combination with the non-penetrating osmoticum polyethylene glycol (PEG). The combined application of ABA and PEG is frequently used to stimulate somatic embryo maturation in a number of conifers (Stasolla et al. 2002) and some angiosperms [e.g. Hevea brasiliensis (Linossier et al. 1997), Corydalis yanhusuo (Sagare et al. 2000), Panax ginseng (Langhansova et al. 2004), etc.]. The practical implementation of somatic embryogenesis and its utilization in encapsulation technology is occasionally limited owing to the asynchronous development of somatic embryos (Ara et al. 2000; Rai et al. 2009a; Vibha et al. 2009). A low concentration of ABA is generally applied for the synchronization of somatic embryos (Bhojwani and Razdan 1996). Among embryo stages, globular embryos respond better to ABA, and somatic embryos appear to become less responsive to ABA during maturation (Vahdati et al. 2006, 2008). ABA-inducible gene expression during somatic embryogenesis Carrot and Arabidopsis are widely used as model plants to study the molecular phenomenon of somatic embryogenesis (Zimmermann 1993; Chugh and Khurana 2002; IkedaIwai et al. 2006). Several cDNAs of ABA-inducible embryo-specific/embryogenic cell proteins, such as LEA proteins, have been isolated from these two plants and characterized (Hatzopoulos et al. 1990; Kiyosue et al. 1992, 1993; Yang et al. 1996, 1997; Zhu et al. 1997; Shiota et al. 1998; Shiota and Kamada 2000). Dc3, Dc8,
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High sucrose
Transition from proliferation to maturation phase
Fig. 2 Transition of somatic embryos from the proliferation to maturation phase and biochemical and morphological changes during this process. a Globular stage somatic embryos, b development of mature (torpedo stage) somatic embryo of guava. LEA Late embryogenesis abundant (proteins)
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Synthesis of storage and LEA proteins Increase desiccation tolerance
Prevent precocious germination
Somatic embryos maturation
DcECP31, DcECP40 and DcEMB1 from carrot and AtECP31 and AtECP63 from Arabidopsis are important ABA-inducible genes that encode LEA proteins and which show increased expression in the mature stage of somatic embryos (Zimmermann 1993; Chugh and Khurana 2002; Ikeda-Iwai et al. 2006; Table 3). ABI3 is involved in the seed-specific signal transduction of ABA (Karami et al. 2009). A homolog of this gene, namely, C-ABI3, which has been isolated from carrot, is expressed in embryogenic tissue and regulates the expression of the ECP genes (Karami et al. 2009). ECP genes, which encode embryogenic cell proteins (ECPs), members of the LEA group of proteins (Kiyosue et al. 1992; Kim et al. 2006), are positively regulated by ABA (Karami et al. 2009). Dong and Dunstan (1997) reported the characterization of five ABAresponsive somatic embryo abundant cDNAs from a gymnosperm white spruce (Picea glauca). Of these five cDNAs, three (PgEMB 12, 14 and 15) were predicted to encode homologs of different LEA proteins. Fischerova et al. (2008) determined the expression of PaVP1, an ortholog of the ABI3 gene, in Picea abies and evaluated the impact of PaVP1 expression on embryo maturation. They concluded that the initiation and maintenance of PaVP1 expression and proper embryo development was influenced by exogenous ABA. In vitro conservation The in vitro conservation of plants for short to medium periods of time through a tissue culture approach can be
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Table 3 A number of the ABA-inducible genes expressed during carrot and Arabidopsis somatic embryogenesis Genes
Functions
References
Daucus carota Hormone-responsive
Kiyosue et al. (1992, 1993), Zhu et al. (1997)
Dc3, Dc8, DcECP31, DcECP40, DcEMB1
DcECP31, DcECP40, DcECP63
LEA proteins
Hatzopoulos et al. (1990), Zimmermann (1993)
C-ABI3
Expression of the ECP genes
Shiota et al. (1998), Shiota and Kamada, 2000)
Arabidopsis thaliana AtECP31, AtECP63
Hormone-responsive
Yang et al. (1996, 1997)
AtABI3
Expression of the LEA genes
Ikeda-Iwai et al. (2002, 2003)
LEA, Late embryogenesis abundant; ECP, embryogenic cell protein For details see the reviews of Zimmermann (1993), Chugh and Khurana (2002), and Karami et al. (2009)
achieved by using various procedures to reduce growth, such as by increasing the interval between subcultures. A well-known approach that is often used for slow-growth conservation is modification of the cultural and/or environmental conditions, such as the maintenance of cultures under reduced temperature and/or reduced light intensity or low oxygen concentration and the use of growth retardants, osmoticum or minimal growth medium (alteration of mineral content and/or sucrose in medium) (Engelmann et al. 2003; Gupta and Mandal 2003; Rai et al. 2008b, 2009b). The use of ABA for in vitro slow-growth conservation has been reported for many plant species (Watt et al. 2000; Gopal et al. 2004; Morata et al. 2006). Generally somatic embryos can not be conserved for long periods due to precocious germination, even at low temperature (Choi and Jeong 2002). However, the application of ABA can artificially induce the quiescent state in somatic embryos, similar to the dormancy state in zygotic embryos, and promote short- to medium-term conservation (Zimmermann 1993). Rai et al. (2008a) recently reported the successful storage of encapsulated somatic embryos of guava by ABA application. Choi and Jeong (2002) also reported that a high concentration of endogenous ABA was accumulated in dormant somatic embryos of Siberian ginseng induced by a high sucrose concentration. Cryopreservation has attracted much attention as a suitable technique for the long-term storage of cultured plant materials and plant genetic resources. In the most applicable methods of cryopreservation, of which vitrification is an example, the induction of high levels of tolerance to desiccation in the tissue is an essential step prior to the immersion of the material in liquid nitrogen (Suzuki et al. 2006). This increased tolerance to desiccation is mostly achieved by preculturing the plant material for 1–7 days in a medium containing a high concentration of sucrose (Engelmann et al. 2003). Different authors have addressed the effect of ABA in the preculture medium on the cryopreservation tolerance in many plants and found that ABA improves the recovery of cryopreserved explants
(Na and Kondo 1996; Ryynanen 1998; Vandenbussche and De Proft 1998; Chang and Reed 2001; Gagliardi et al. 2003; Fang et al. 2004; Beardmore and Whittle 2005; Suzuki et al. 2006; Burritt 2008; Popova et al. 2009). The exogenous application of ABA has been associated to protein synthesis and compatible solutes which play an important role in freezing tolerance (Stewart and Voetberg 1985; Fang et al. 2004). Stress tolerance In the last 20–30 years, many papers have been published on the role of plant tissue culture on stress tolerance and the development of stress-tolerant plants through in vitro selection (Purohit et al. 1998; Rai et al. 2011). Endogenous ABA levels significantly increase in response to environmental stresses, and they regulate some aspects of physiological responses to a variety of environmental stresses (Mongrand et al. 2003; Schwartz et al. 2003; Xiong and Zhu 2003; Tuteja 2007). Many authors also report that both the adaptation and survival of plant cells and tissues to various environmental stresses may be enhanced by exogenous ABA (Chen and Gusta 1983; LaRosa et al. 1985, 1987; Reaney and Gusta 1987; Eberhardt and Wegmann 1989; Bartels et al. 1990; Churchill et al. 1992; Lee et al. 1992; Arora and Wisniewski 1995; Rajashekar and Lafta 1996; Mills et al. 2001; Parmentier-Line et al. 2002; Ding et al. 2010). Acclimatization of tissue culture-raised plants The extensive use of micropropagation is restricted by the high percentage of plants lost or damaged when the cultured plants are transferred to ex vitro conditions. Under in vitro culture conditions, plants grow under low irradiance levels, aseptic conditions, on a medium containing sufficient sugar and nutrients to allow for heterotrophic growth and in an atmosphere with a high level of humidity. These conditions lead to the formation of plantlets that differ in
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terms of morphology, anatomy and physiology from naturally growing plants, resulting in poor survival under natural environmental conditions when they are directly transferred from the in vitro conditions (Pospisilova et al. 2007). Acclimatization of micropropagated plantlets to the natural environment requires several morphological, anatomical and physiological changes, as highlighted in a number of recent reviews (Pospisilova et al. 1999, 2007; Hazarika 2003). ABA acts as an anti-transpirant during the acclimatization of tissue culture-raised plantlets and reduces the relative water loss of the leaves of micropropagated plantlets during transplantation even when non-functional stomata are present (Pospisilova et al. 1999, 2007). Pospisilova et al. (2009) recently reported that the addition of ABA to the last subculture improved the survival rate of tobacco plantlets transferred to the natural environmental conditions. Acclimatization can also be improved by the positive effect of ABA on Chlorophyll a content and other photosynthetic parameters as well as on plant growth (Pospisilova et al. 1999, 2007). A number of other reports also document the significant role of ABA in the acclimatization of tissue culture-raised plants (Aguilar et al. 2000; Hronkova et al. 2003). ABA reduces programmed cell death in cultured cells and tissues Programmed cell death (PCD), also known as apoptosis, is a physiological cell death process in which a cell guides its own destruction (Pennell and Lamb 1997; Wang et al. 1999; Carimi et al. 2003). In plants, it has been proven that certain fungal infections and environmental stresses can induce PCD (Gilchrist 1998; Wang et al. 1999). Fragmentation of DNA into oligomers due to intra-nucleosomal cleavage, a known characteristic of PCD, was observed in anther culture of Hordeum vulgare by Wang et al. (1999). They subsequently suggested that pretreatment with exogenous ABA would be effective in stimulating androgenesis and protecting microspores from dying by apoptosis. In another study, Carimi et al. (2003) reported that a high concentration of cytokinin blocks cell proliferation and induces PCD in cell culture of Arabidopsis and carrot. In order to reduce cytokinin-induced PCD, they added exogenous ABA into the culture medium along with 6-benzylaminopurine (BAP) and found that ABA protects cells against BAP-induced cell death.
Concluding remarks There are several lines of evidence suggesting that ABA may not only be involved in somatic embryo maturation and in vitro conservation but that it may play a significant
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role in the in vitro stress tolerance and acclimatization of tissue culture-raised plantlets. Considerable progress has been made during the last 20–30 years on identifying and characterizing the molecular mechanisms and regulation of somatic embryo maturation by ABA; however, such findings are mostly restricted to model plants, such as carrot or Arabidopsis. Most researchers believe that ABA regulates the synthesis of storage and LEA proteins in somatic embryos, resulting in their maturation. However, a number of recent reports have linked the maturation of somatic embryos with antioxidative enzymes or H2O2 generated by the exogenous application of ABA—although the molecular mechanisms are still unknown. Ongoing research projects carried out in many laboratories worldwide are expected to solve some key questions regarding the actual mechanism of ABA-based somatic embryo maturation. ABA has also received much attention for their involvement in abiotic tolerance and disease resistance. The results of such studies suggest that ABA could be applied as an alternative selection agent for the development of stresstolerant plants through in vitro selection. Acknowledgments The authors (M.K. Rai and Harish) wish to acknowledge to University Grants Commission (UGC), New Delhi for the award of the Dr. D.S. Kothari Post Doctoral Fellowship. We are also grateful to the Department of Biotechnology (DBT), Department of Science and Technology (DST), Council of Scientific and Industrial Research (CSIR) and University Grants Commission (UGC), New Delhi for financial support. Valuable suggestions by the anonymous reviewers for improving the manuscript are also very much appreciated.
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