Regulating Gene Expression in High-scale Plants Micropropagation
Ariel D. Arencibia,
Signaling mechanisms have been elicitated towards the priming and biopriming stages during micropropagation in Temporary Immersion Bioreactors (TIBs) in sugarcane as model plant. CO2-rich TIBs induces a photomixotrophic condition adequate for the production of natural phenolic metabolites, altogether increasing multiplication rates and functional plants rooting. When combined with Gluconacetobacter diazotrophicus inoculations during transplanting, originate a significant improvement of the percentage of plant adaptability to natural conditions. A more efficient micropropagation process has been optimized on the basis of an accurate exploitation of the natural plant physiology.
Received: August 18, 2011;
Accepted: November 17, 2011;
Published: January 03, 2012
Plant tissue culture refers to growing and multiplication of cells, tissues
and organs on defined solid or liquid media under aseptic and controlled environment.
Forty years of in vitro plant research has delivered many well-developed
systems that are routinely applied to scientific and commercial activities,
namely: (a) micropropagation of genotypes; (b) production of disease-free material
from excised apical meristems; © international germplasm exchange; (d)
generation of somaclones; (e) rapid disease and pest resistance screening; and
(f) germplasm conservation (Snyman et al., 2011).
Plant micropropagation procedures are conducted under conditions as natural
or similar to those in which the plants will be ultimately grown ex vitro
(Ahloowalia et al., 2004). The individual plant
species, varieties and clones require specific modification of the growth media,
weaning and hardening conditions. In general, the process of plant micropropagation
is universally divided into well-defined stages depending on genotype/specie
Network discovery is a generic term describing the effort of elucidating the
nature of relationships between molecules and associated properties emerging
from of a biological network. Multiple types of networks have been described
with respect to the types of molecules involved and the dimension of the molecular
network (Weitz et al., 2007). Similar efforts
are under way to construct plant transcriptional regulatory networks, for example
those that control flower and root development (Grieneisen
et al., 2007), photomorphogenesis (Jiao et
al., 2007; Nemhauser, 2008) or the circadian
clock (Zeilinger et al., 2006).
Technological advances in biological experimentation are now enabling researchers
to investigate living systems on an unprecedented scale by studying genomes,
proteomes or molecular networks in their entirety. Whether gene expression analysis
provide a rich source of quantitative biological information that allows researchers
to move beyond a reductionist approach by both integrating and understanding
interactions between multiple components in cells, organisms and processes (Baginsky
et al., 2010).
This study considers plant micropropagation as a complex physiological network where each step must believe as an independent one, i.e., establishment, multiplication, rooting, adaptation to field conditions, etc. Integration/management of gene expression systems in parts of the entire micropropagation process (network) have been conducted in sugarcane as model plant. Regulations of gene expression towards useful traits increase the productive efficiency during plant micropropagation integrating both basic and applied researches.
Temporary Immersion Bioreactors (TIBs): Bioreactors are vessels designed
for large-scale cell, tissue or organ culture in liquid media. A more precise
control of the plant growth gaseous exchange, illumination, medium agitation,
temperature and pH than the conventional culture vessels is providing by bioreactors
increasing the multiplication rates and growth of plant cultures (Levin
and Tanny, 2004; Paek et al., 2005). The
environment of the growth room determines the light, temperature and gases in
the bioreactor vessels (Morini and Melai, 2004).
In temporary immersion bioreactors, the cultures are immersed in the medium,
for a preset duration at specified intervals in dependence of plant species
and genotypes (Adelberg and Simpson, 2002; Debnath,
2011). TIBs demonstrate a positive effect on plant physiology regulating
key pathways as photosynthesis, respiration, transport and nutrient assimilation.
As consequences both cell development and cell division rates are significantly
enhanced (Etienne and Berthouly, 2002). Environmental
factors influencing plant physiology, including the presence of systemic microorganisms
(benefic, pathogenic and contaminants), during plant micropropagation are show
in Fig. 1.
The influence of these environmental factors on plant physiology could be considered
similar to those for conventional micropropagation. Nevertheless, key differences
with the time and quality of the exposure are demonstrated throughout the interactions.
|| Factors influencing plant micropropagation in Temporary Immersion
Other significant difference is the improved availability to manipulate or
regulate, the interactions using automatic devices. For superior practical use
of bioreactor cultures, research aimed at improving the physical and chemical
environments-such as increased air exchange, increased Photosynthetic Photon
Flux (PPF) and optimized CO2 content are necessary (Paek
et al., 2001; Morini and Melai, 2004).
Prevention of contamination in bioreactors requires a proper handling of the
plant material, of equipment during transfers and cultures during production.
Culture contamination which is a major problem in conventional commercial micropropagation,
is even more acute in TIBs (Leifert, 2000). Only the
surface sterilized explants, indexed as diseases-free must be used to initiate
cultures in bioreactors. However, despite the precautions taken in initiating
cultures, bioreactors can become contaminated from the environmental microbes.
It is noticeable that photomixotrophic plant cultures show a significant diminution
or even control of environmental contamination which could be also associated
with the significant reduction of sucrose in the culture medium and the production
of natural bioactive phytomolecules (Sivakumar, 2006;
Arencibia et al., 2008).
Considering the main advantages and disadvantages, the use of bioreactors has
led to the development of suitable technologies for plant propagation. Currently,
various plant species as sugarcane, pineapple, banana, between others, are propagated
using bioreactors to certified seeds production (Escalona
et al., 1999, 2003; Ibaraki
and Kurata, 2001; Etienne and Berthouly, 2002; Chakrabarty
et al., 2003; Arencibia et al., 2008).
Priming: One of the important plant adaptations to complex environment
challenges is priming behavior (Conrath et al., 2006;
Beckers and Conrath, 2007; Frost
et al., 2008). In principle, priming means that plants that previously
experienced abiotic or biotic stress have altered and most often enhanced their
ability to resist and survive recurring stress conditions. In the current terminology,
priming is usually associated with biotic stresses while hardening
is used for response adaptations of plants to abiotic factors (Bruce
et al., 2007). Priming effects span trophic levels: plants can be
primed by herbivore attack, pathogen infection and colonization with micro-organisms,
exposure to the metabolites these organisms produce and even synthetic compounds
(Conrath et al., 2001).
Conrath et al. (2001) proposed that the accumulation
of signaling proteins in their inactive form and their rapid activation in new
stress situations can contribute to the formation of short-term stress imprints.
Protein phosphorylation and dephosphorylation is one of the most important reversible
post-translational modifications that causes inactive proteins to become active
and vice versa (Van Bentem and Hirt, 2007). Members of a diverse class of Mitogen
Activated Protein Kinases (MAPK) are known to play important roles in mediating
pathogen resistance as well as in JA-dependent signal transduction cascades
(Seo et al., 2007; Takahashi
et al., 2007; Wu et al., 2007; Iriti
et al., 2007). A concrete example in Arabidopsis shows that
the priming competence induced by treatment with salicylic acid analog benzo
(1,2,3) thiadiazole-7-carbothioic acid S-methyl ester (BTH), sold under trade
name BionTM (Syngenta AG, Basel, Switzerland) and used commercially for priming
and protecting crops against plant pathogens (Iriti et
al., 2007), can be attributed to the accumulation of inactive MPK3 proteins
(Conrath et al., 2006); these are activated in
response to pathogen infection, thereby enhancing the expression of defense
genes and the accumulation of antifungal metabolites.
In addition, more permanent but still reversible changes in gene expression-namely
those involved in protection from stress-have been described in plants. In particular,
DNA methylation (Mathieu et al., 2007), histone
modifications and changes in small-RNA (smRNAs) populations play a role in plant
defense-related memory mechanisms. Pandey and Baldwin (2008)
can lead to heritable or transgenerational alterations in plant behavior, some
of which cannot be explained by Mendelian genetics. Readers are directed to
examples of several current reviews that analyze the broad areas of DNA and
histone modifications in epigenetic control of development and stress responses
(Bronner et al., 2007; Boyko
and Kovalchuk, 2008).
Phenolic metabolites as priming molecules: Sugarcane, a major source
of world sugar and bioenergy production (Waclawovsky et
al., 2010), is growing throughout the tropics and subtropics. In this
sense, as all major plant-based industries require extensive breeding programs
to produce/introduce improved genotypes (e.g., sugar content) that are matched
to specific selection sites, accounting for biotic (e.g., pest and disease resistance)
and abiotic factors in each part of the world (Snyman et
The use of temporary immersion systems in sugarcane promoted both phenolic
excretion and shoots formation (Lorenzo et al., 2001).
In this way, a genomic characterization of plants has been achieved by suppressing
key genes of the phenylpropanoid pathway; as a result, a new function of phenolic
metabolites as priming molecules has been characterized during sugarcane micropropagation
in TIBs. Genes related to cell metabolism and development (10), plant defenses
(9), phenylpropanoids (7), methyl jasmonate response (5), ethylene (5), oxidative
burst (3) and auxins (3) pathways, among others (8) were found to be induced
in sugarcane plants micropropagating in TIBs with phenolic metabolites, supporting
that phenylpropanoids might act as elicitor molecules of others biochemical
pathways (Arencibia et al., 2008). As conclusion
phenolics related to the brown color in the culture medium display a beneficial
role for the induction/expression of genes during sugarcane propagated in TIBs.
The priming approach has been integrated into the sugarcane micropropagation
technology by TIBs. Sugarcane micropropagation in CO2-rich TIBs induces
a mixotrophic condition adequate for the production of natural phenolic metabolites
(Fig. 2a). Scaling up has been conducted in several commercial
genotypes. While phenolics demonstrate to act as priming molecules during the
in vitro culture, vitroplantlets growing and shooting in the presence
of phenolic metabolites display an enhanced vigor measured as plant size (Fig.
2b,c), emitted functional roots and increase adaptability
to the natural environment. Additionally, when combined with the inoculation
of the endophytic Gluconacetobacter diazotrophicus, a significant improvement
of the percentage of survival has been attached through this critical step (Arencibia
et al., 2008; Bernal et al., 2008).
Sugarcane phenolic metabolites as elicitors of resistance to tomato bacterial
wilt in the Solanum lycopersicum and Ralstonia solanacearum pathosystem
has also been identified (Yang et al., 2010).
The culture media was collected and the phenolics were sprayed onto tomato plants
infected with R. solanacearum, eliciting and/or maintaining an early
defense signaling mechanism that resulted in the protection of the plant against
the tomato bacterial wilt disease. RT-PCR analyses confirmed that selected genes
from defense-related pathways were differentially expressed between plants treated
with sugarcane metabolites, non-treated pathogen-free plants and non-treated
plants inoculated with R. solanacearum (Yang et
al., 2010). Results indicate a promising potential for diversification
of the sugarcane micropropagation industry by the production of useful phenolic
metabolites as byproducts.
The phenylpropanoid pathway is an important pathway in secondary plant metabolism,
yielding a variety of phenolics with structural and defense related functions.
These phenolic compounds include lignins, phenolic acids, flavonoids and stilbenes.
In addition, enzymes such as phenylalanine ammonialyase (PAL; EC 18.104.22.168), cinnamate-4-hydroxylase
(C4H; EC 22.214.171.124) and 4-coumarate:coenzyme A ligase (4CL, EC 126.96.36.199) are
considered to be crucial to phenylpropanoid metabolism. A number of reports
have shown that phenylpropanoid derivatives are capable of protecting plants
against various biotic (infection by viruses, bacteria, fungi) and abiotic (low
and high temperatures, UV-B light, wounding) stresses (Sgarbi
et al., 2003; Solecka and Kacperska, 2003).
Stilbene synthase (STS) (EC 188.8.131.52) catalyses the last step of the phenylpropanoid
biosynthesis pathway leading to the formation of stilbene phytoalexins. Expression
of STS genes is often induced in response to biotic and abiotic stresses (Jeandet
et al., 2002).
Beside, BABA (beta aminobutyric acid) a non-protein amino acid, was used to
induce resistance in grapevine against downy mildew (Slaughter
et al., 2008). BABA-induced resistance was observed in the susceptible
cv. Chasselas as well as in the resistant cv. Solaris. Following BABA treatment,
sporulation of Plasmopara viticola was strongly reduced and the accumulation
of stilbenes increased with time following infection. Furthermore, BABA-treatment
of Solaris led to a rapid increase in transcript levels of three genes involved
in the phenylpropanoid pathway: phenylalanine ammonialyase, cinnamate-4-hydroxylase
and stilbene synthase. BABA-primed Chasselas showed increased transcript levels
for cinnamate-4-hydroxylase and stilbene synthase. As a result, the susceptible
cultivar became more resistant to downy mildew. In parallel, in grapevine, it
has been shown that callose deposition as well as defense mechanisms depending
on the phenylpropanoid and the Jasmonic Acid (JA) pathways all contributed to
BABA-IR (Hamiduzzaman et al., 2005).
Biopriming: Many symbiotic organisms contribute to the vigor and ability of the tissue-cultured plants to perform well in the field. In the course of tissue culture, plants are made free from such beneficial microbes, e.g., symbiotic nitrogen fixing endophytic bacteria and mycorrhizae. There is no practical way to retain the beneficial microorganisms during tissue culture. The deliberate re-infection of propagules with selected strains can be a valid way of retrieving the benefits of such microbes as a biopriming approach.
Endophytic microorganisms can promote plant growth, as well as suppress diseases.
Plant growth promotion is taken to result from improved nutrient acquisition
or hormonal stimulation (Suman et al., 2005).
Disease suppression can occur through induction of resistance in the plant (Arencibia
et al., 2006).
Several bacterial strains have been shown to act as plant growth-promoting
bacteria (PGPR) through both stimulation of growth and Induced Systemic Resistance
(ISR) but it is not clear in how far both mechanisms are connected. Induced
resistance is manifested as a reduction of the number of diseased plants or
in disease severity upon subsequent infection by a pathogen. Such reduced disease
susceptibility can be local or systemic, result from developmental or environmental
factors and depend on multiple mechanisms (Van Loon, 2007).
The spectrum of diseases to which PGPR elicited ISR confers enhanced resistance
overlaps partly with that of pathogen-induced Systemic Acquired Resistance (SAR).
Although ISR-eliciting bacteria can induce typical early defense-related responses
in cell suspensions, in plants they do not necessarily activate defense-related
gene expression. Instead, they appear to act through priming of effective resistance
mechanisms, as reflected by earlier and stronger defense reactions once infection
occurs (Van Loon, 2007).
While, these bacteria utilize the nutrients that are released from the host
for their growth, they also secrete metabolites. Several of these metabolites
can act as signaling compounds that are perceived by neighboring cells within
the same micro-colony, by cells of other bacteria that are present or by cells
of the host plant (Van Loon and Bakker, 2003; Bais
et al., 2004; Gray and Smith, 2005; Kiely
et al., 2006).
The specificity in the reactions of different plant species to individual strains
indicates that the reactions of plants to resistance-inducing PGPR must be the
outcome of a dynamic interplay between the production and the perception of
ISR eliciting signals. Whereas, some PGPR activate defence-related gene expression,
others appear to act solely through priming of effective resistance mechanisms,
as reflected by earlier and stronger defence reactions once infection occurs
(Gray and Smith, 2005; Kiely et
Gluconacetobacter diazotrophicus as biopriming: Gluconacetobacter
diazotrophicus, Herbaspirillum sp., Azospirillum amazonense,
Burkholderia spp., capable of fixing nitrogen have been reported to colonize
the epidermis of sugarcane stem and roots, of which Gluconacetobacter (earlier
Acetobacter diazotrophicus) seems to contribute substantially to nitrogen
nutrition of the plant (Dobereiner et al., 1993;
James et al., 2001). Gluconacetobacter diazotrophicus,
a nitrogen fixing endophyte, is found in high number in all part of sugarcane
and its better colonization in sugarcane is probably due to its capability to
grow in the presence of high sugar and low pH (Dobereiner
et al., 1993).
Production of plant growth hormones is the other beneficial trait associated
with Gluconacetobacter diazotrophicus (Bastin et
al., 1998; James et al., 2001). The exact
role of such endophytic colonization individually or in a complex endophytic
community is not yet very clear but inoculation experiments involving micropropagated
plants suggest the positive colonization and its contribution to plant growth
and development in terms of improved plant height, nitrogenase activity, leaf
nitrogen, biomass and yield (Dobereiner et al., 1993;
Sevilla et al., 2001; Muthukumarasamy
et al., 2002).
More recently, a new role for the plant growth-promoting nitrogen-fixing endophytic
bacteria Gluconacetobacter diazotrophicus has been identified and characterized
while it is involved in the sugarcane-Xanthomonas albilineans pathogenic
interactions. Living G. diazotrophicus possess and/or produce elicitor
molecules which activate the sugarcane defense response resulting in the plant
resistance to X. albilineans, in this particular case controlling the
pathogen transmission to emerging agamic shoots. A total of 47 differentially
expressed transcript derived fragments (TDFs) were identified by cDNA-AFLP.
Transcripts showed significant homologies to genes of the ethylene signaling
pathway (26%), proteins regulates by auxins (9%), β-1,3 Glucanase proteins
(6%) and ubiquitin genes (4%), all major signaling mechanisms. Results point
toward a form of induction of systemic resistance in sugarcane, G. diazotrophicus
interactions which protect the plant against X. albilineans attack (Arencibia
et al., 2006).
Biopriming approach has also been integrated into the sugarcane micropropagation
technology by Temporary Immersion Bioreactors (TIBs). While phenolics demonstrate
to enhance plant capability to be colonized by the endophytic Gluconacetobacter
diazotrophicus, a simple procedure for G. diazotrophicus inoculation
has been developed using sugarcane vitroplants during transplanting (Fig.
2d, e). As result a significant improvement of the percentage
of adaptability and plant growth rate have been demonstrated in high scale plants
micropropagation (Bernal et al., 2008).
||Large-scale sugarcane micropropagation in (a) CO2-rich
TIBs, (b) induction of a functional rooting during the last in vitro
step as an evidence of the photomixotrophic stage, (c-d) sugarcane vitroplantlets
obtained in a TIB using 5 L of the culture medium, (e) inoculation of vitroplantlets
with a suspension of G. diazotrophicus and planting in a soil-compost-zeolite
mixture and (f) twenty-days olds sugarcane plants adapted to the natural
Besides sugarcane, Gluconacetobacter diazotrophicus colonizes many
other sugar and non-sugar plants like Pennisetum purpureum, Ipomea
batatas Döbereiner, Coffea arabica (Jimenez-Salgado
et al., 1997), Eleusine coracana (Loganathan
et al., 1999) and Ananas comosus (Tapia-Hernandez
et al., 2000). Present strategy could be applied to other plants
from which recently Gluconacetobacter diazotrophicus has also been isolated
(Cocking et al., 2006), i.e., Arabidopsis
thaliana and the crop plants maize (Zea mays), rice (Oryza sativa),
wheat (Triticum aestivum), oilseed rape (Brassica napus), tomato
(Lycopersicon esculentum) and white clover (Trifolium repens).
For a bioinoculant to benefit the plant, it should establish and compete with
the native heterotrophic bacterial population and also should acclimatize the
local conditions. Under such conditions the indigenous bioinoculant strains
may perform better than introduced alien ones for promoting plant growth due
to their superior adaptability to the environment. Therefore, selection of superior
strains of Gluconacetobacter diazotrophicus is essential for its exploitation
as bioinoculant for improving growth of in vitro sugarcane plants (Oliveira
et al., 2002).
As summary views of the sugarcane micropropagation process is show in Fig. 2.
An assessment between the conventional micropropagation technology (agar base) and the new one including CO2-rich TIBs producing phenolics and a further inoculation with G. diazotrophicus is show in Table 1. The crucial steps influencing the main parameters related to productive efficiency are under layer considering the conventional micropropagation as the comparison base.
|| Comparing high-scale plant micropropagation technologies
in sugarcane as model plant
|| The optimization for photomixotrophic conditions is required
in a case by case manner using the TIBs as a plant multiplication platform.
A permanent goal must be reach the whole autotrophic stage at least in the
final in vitro stage
||Wherever possible, the priming and biopriming strategies should be standardized
according to local conditions, as well as considering the specific plant-microbe
||The integration of new approaches for plant micropropagation should result
in a more efficient and competitive technology, where both basic and applied
researches must be primarily focused to take profit of the natural plant
physiology during the in vitro stage
To Sugar Ministry and CITMA, Cuba, for supports this work. Thanks to researchers and technicians staffs at Genetic and Phytopathology Program, National Institute for Sugarcane Research, Cuba.
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